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)

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

To my family.

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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.

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

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

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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 development, reproduction and transmission. Negative effects of forest edges, fragmentation and small habitat size on parasite prevalences can be most likely attributed to similarly altered vegetation. Parasite life cycle traits such as long environmental periods, free living generations or the dependence on arthropod intermediate hosts were suggested to increase parasite susceptibility to the mentioned environmental changes. However, ectoparasites like stationary sucking lice and nest-associated Laelaptidae mites also exhibited negative responses, although those appeared to be buffered by their host-associated lifestyle. On the other end of the response spectrum, some directly transmitted and homoxenous parasites

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(pinworms and Atopomelidae mites) were not strongly affected by environmental changes. Variabilities in their prevalences could rather be explained by host-related factors like sex and body condition. However, pinworm prevalences (Enterobiinae gen. sp., Lemuricola sp.) were responding differently to the factor forest maturation, which could not be fully clarified. With the identification of important parasite and habitat characteristics mediating parasite-host- habitat interactions in a fragmented ecosystem, the results of this work provide new insights with respect to the previously underestimated vulnerability of parasite diversity to anthropogenic environmental change.

Zusammenfassung

Frederik Kiene (2021)

Auswirkungen von Habitatfragmentierung auf Parasiteninfektionen von Mausmakis (Microcebus spp.) und anderen Kleinsäugern aus Nordwestmadagaskar Durch den stetig wachsenden Hunger der Menschheit nach Ressourcen geraten Ökosysteme weltweit immer stärker unter Druck und sind derzeit enormen Veränderungen unterworfen. Die Fragmentierung natürlicher Lebensräume spielt dabei eine besonders wesentliche Rolle. Obwohl Parasiten elementare Bestandteile eines jeden Ökosystems sind, wurden Einflüsse einer fragmentierten Umwelt auf diese bisher kaum erforscht. In der vorliegen Arbeit wurden daher zehn verschiedene Wirts- und Habitatfaktoren in einem fragmentierten Trockenwaldökosystem auf ihre Auswirkungen auf Ekto- und Magen-Darm- Parasiteninfektionen von mehr als 900 Individuen vier verschiedener Kleinsäugerarten (zwei Primatenarten - Microcebus murinus und M. ravelobensis; zwei Nagerarten - Eliurus myoxinus [endemisch] und Rattus rattus [invasiv]) in Nordwestmadagaskar untersucht. Der Befall dieser Wirte mit Zecken (Haemaphysalis microcebi), verschiedenen Milben (Trombiculidae, Laelaptidae, Atopomelidae), Läusen (Lemurpediculus spp., Polyplax sp., Hoplopleura sp.) und verschiedenen Nematoden (Enterobiinae gen. sp., Lemuricola sp., Strongyloides spp., Subuluroidea fam. gen. spp. und Spirurida) wurde dabei mittels verallgemeinerten linearen gemischten Modellen genauer im Hinblick auf die Effekte einzelner Faktoren analysiert. Die Ergebnisse deuten auf einen negativen Zusammenhang zwischen den Prävalenzen vieler Parasitenarten und Vegetationsveränderungen im Kontext von Habitatfragmentierung hin. Insbesondere temporäre Ektoparasiten (Zecken, Milben der Familie Trombiculidae), heteroxene Parasiten (Subuluroidea fam. gen. spp., spirurider Eityp 1) und Arten mit heterogonen freilebenden Generationen (Strongyloides spp.) waren betroffen. Heißeres und trockeneres Mikroklima mit einem Mangel an organischem Material im Bodengrund wirken sich in Gebieten mit offener Vegetation vermutlich negativ auf Entwicklung, Vermehrung und Übertragung der beeinträchtigten Parasitentypen aus. Auch geringere Parasitenprävalenzen im Zusammenhang mit Waldrändern, Fragmentierung und geringer Größe von Habitatfragmenten können höchstwahrscheinlich auf eine ähnlich veränderte Vegetation zurückgeführt werden. Es wird angenommen, dass Merkmale der Parasitenzyklen wie lange Umweltperioden, frei lebende Generationen oder die Abhängigkeit von Arthropoden als Zwischenwirt die Anfälligkeit der Parasiten gegenüber den genannten

Umweltveränderungen erhöhen. Es zeigten sich jedoch auch Ektoparasiten wie stationäre Läuse und nestassoziierte Milben der Familie Laelaptidae negativ durch Waldrandeffekte und Fragmentierung beeinflusst, die Effekte schienen aber durch ihre wirtsassoziierte Lebensweise abgemildert zu sein. Andere direkt übertragene und homoxene Parasiten (Pfriemenschwänze und Milben der Familie Atopomelidae) waren nicht so stark von Umweltveränderungen betroffen. Veränderungen in ihren Prävalenzen konnten eher durch wirtsbezogene Faktoren wie Geschlecht und Körperkondition erklärt werden. Pfriemenschwänze (Enterobiinae gen. sp., Lemuricola sp.) reagierten jedoch unterschiedlich auf den Faktor „Waldmaturation“, was nicht vollständig geklärt werden konnte. Die Ergebnisse dieser Arbeit bieten neue Erkenntnisse im Hinblick auf die bisher unterschätzte Verwundbarkeit der Parasitendiversität gegenüber anthropogenen Umweltveränderungen und identifizieren dabei wichtige Merkmale von Parasit und Habitat als Haupteinflussfaktoren in diesem Zusammenhang.

1 General introduction The global human population, reaching a number of 7.7 billion in 2019, doubled within the last 50 years. Population growth is still proceeding and will approach between 9.4 and 12.7 billion by the year 2100 (Goujon, 2018; United Nations, 2019). Simultaneously, the human demand for food and resources grows, being increasingly served at the expense of natural ecosystems. As a consequence, 75% of the Earth´s ice-free terrain is now modified by man (Watson et al., 2016) and particularly countries with high levels of food insecurity exhibit severe levels of natural habitat conversion (Molotoks et al., 2017). Tropical forests, the most species diverse terrestrial habitats on earth (Giam, 2017), are particularly affected (Achard et al., 2002). Estimates describing the worldwide annual loss of natural forest area since the 1990s are ranging between 0.5 and 5.9 % (Hansen et al., 2010; Keenan et al., 2015). The loss of natural vegetation is typically associated with high degrees of fragmentation and degradation (Fletcher et al., 2018). It has been estimated that over 95% of the remaining forest patches worldwide are smaller than 250 ha (Ribeiro et al., 2009) and more than 70% of the remaining forest area is located within 1000 m to the closest forest edge (Haddad et al., 2015). Because of the strong ecological specialization of many species and the inability to adapt quickly enough to the rapidly changing environmental conditions, negative consequences for biodiversity are substantial (Pereira et al., 2010). Projected rates of species loss are severe and the consequences of this development also pose threats to human existence (Cardinale et al., 2012). The loss of natural habitats and the extinction of key species leads to a reduction of biomass and altered nutrient flows. Essential ecosystem services that ensure hydrological cycles, detoxification, soil formation, pollination and the global climate, also permitting human life, may become impaired or entirely lost (Haddad et al., 2015; Hooper et al., 2012; Ibáñez et al., 2014).

1.1 Habitat fragmentation – implications for biodiversity With numerous studies relating the continuous decline of species diversity to globally shrinking and fragmented natural ecosystems, the literature on effects of habitat loss and fragmentation on biodiversity is extensive (Fahrig, 2002; Hanski, 2011; Pardini et al., 2017). Impacts of environmental changes by HF were shown and profoundly explained for many species of taxonomic groups including mammals (Andren, 1994; Andriatsitohaina et al., 2020b; Crooks et al., 2017, 2011; Goodman and Rakotondravony, 2000; Klass et al., 2020; Steffens, 2017), birds (Andren, 1994; Herkert, 1994; Watson et al., 2005), amphibians (Cushman, 2006; Hager, 1998; Kolozsvary and Swihart, 1999), reptiles (Hager, 1998; Mac

Nally and Brown, 2001), invertebrates (Didham, 1997; Niemelä, 2001), fungi (Vannette et al., 2016) as well as vascular (Ibáñez et al., 2014; Raghubanshi and Tripathi, 2009; Tabarelli et al., 1999; Young et al., 1996) and non-vascular plants (Wilson & Provan, 2003). While negative impacts of habitat loss are self-evident, ecologists still disagree if habitat fragmentation (HF) per se has negative effects on biodiversity (Fletcher et al., 2018; Haddad et al., 2015) or whether habitat loss alone is responsible for species decline (Fahrig, 2017; Fahrig et al., 2018). The question if HF can be separated and considered in isolation from habitat loss, is the crucial aspect in this debate. Studies on the effects of HF are further challenged by the complex interplay of the concomitant factors patch size, isolation and the proportion of habitat edges that can all affect habitats and wildlife in various ways. As most studies in the field of HF research (Fletcher et al., 2018), this work will investigate the effects of HF by focusing on a suite of such relevant cofactors. One cofactor of great relevance for the understanding of HF is the reduction of patch size. Species-area relationships (SARs) are a widely used framework to describe biodiversity patterns in ecosystems (Strona and Fattorini, 2014). On the basis of the theory of island biogeography (Wilson and MacArthur, 1967), this relationship is explained by considering species richness as a function of the immigration and extinction rates of species (Simberloff, 1972). Since smaller areas of habitat provide less resources than larger areas, species population sizes should be smaller in smaller areas and larger in larger areas. If migration is restricted by isolation, higher probabilities of species extinction for smaller populations entail a lower species richness in habitats of small size (Connor & McCoy, 1979; Hanski et al., 1996). A positive association between habitat size and species richness has been shown in many studies, in particular for vascular plants (e.g. Zurlini et al., 2002), birds (e.g. Bolger et al., 1991) and mammals (e.g. Lomolino, 1982). However, SAR curves differ in steepness of the slopes, based on the examined group of organisms and type of habitat (Drakare et al., 2006). Another important cofactor of HF is the degree of isolation or connectivity between habitat patches. Local species persistence as well as metapopulation viability depend on immigrations and thereby habitat connectivity to compensate incidental local extinctions by recolonization (Gilbert-Norton et al., 2010; Hanski, 1999). Since individual species differ in their ability to move between habitat patches, the level of connectivity cannot be determined for entire habitats but on the level of species in a particular landscape. This species-individual ability, for instance, is different for a bird, able to fly, than for an arboreal mammal. Connectivity is hence determined by the availability of dispersing individuals of a species and their general 3 vagility within the type of landscape separating patches of suitable habitat (Kindlmann and Burel, 2008). The third important cofactor in the context of HF is the proportion of habitat edges in patches of different size. Habitat edges are interfaces between two different habitat types (e.g. savannah and forest) and create transition zones where different ecosystems border on each other and energy and nutrients are exchanged (Murcia, 1995). The effects of such rather abrupt transitions, so called “edge effects”, extend into both adjacent ecosystems. The majority of edge effects in tropical forest is estimated to penetrate less than 150 m into the forest ( Laurance, 2000; Lenz et al., 2014). However, a significantly higher density of invasive plant species in an Australian rainforest was reported to occur up to a distance of 500 m (Laurance, 1991), which illustrates that edge effects can greatly vary in dimension. Patches of habitat may even suffer from additive edge effects acting on the habitat from different directions (Malcolm et al., 2016) with the result that no unaffected habitat may remain if patch size declines to a certain threshold (Laurance and Yensen, 1991). A distinction can be made between abiotic, direct biotic and indirect biotic edge effects, which, however, are often also mutually dependent (Murcia, 1995). Increased solar radiation (abiotic), for instance, can promote the growth of vegetation (direct biotic) at edges, which in turn influences the microclimate on the ground and interactions within soil species communities (indirect biotic). In a meta-analysis of impacts of forest edges on the abundance of vertebrates, Pfeifer et al. (2017) could show that 85% of the investigated species were affected, 46% positively and 39% negatively. Negatively affected species were more likely to be listed as threatened by the IUCN. Edge effects are generally regarded as promoters of generalist species, which are able to thrive in the transition zone, while habitat specialists are often not able to rapidly adapt to the changed conditions or are replaced by generalists (Mills, 1995; Pfeifer et al., 2017; Ries et al., 2004). The more two adjacent landscapes differ from each other, the more drastic are the ecological changes. Edge effects are hence strongly affecting fragmented forest habitats which are surrounded by open landscapes, e.g., agricultural fields or grassland (Haddad et al., 2015). In addition to the three previously mentioned primary cofactors, HF is often secondarily associated to the degradation of habitat (Scanes, 2018). This describes “a set of processes by which habitat quality is reduced” (Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services, 2019). Although natural factors like drought, aridification and cold temperatures might lead to habitat degradation, predominantly human activities like forestry, hunting, animal husbandry, mining and settlements are responsible for habitat degradation in

4 fragmented habitats (Scanes, 2018). In forest ecosystems, habitat degradation is mostly linked to changes in vegetation structure like decreasing canopy cover, tree and understory density (Brooks and Kyker-Snowman, 2008; Wang et al., 2005). Also plant community composition changes and plant diversity decreases (Raghubanshi and Tripathi, 2009). Consequences for animals living in those habitats are related to the availability of resources like food and shelter (Andrianasolo et al., 2006), but secondary mechanisms might also lead to a change of abiotic conditions like temperature and humidity (Brooks and Kyker-Snowman, 2008; Hillers et al., 2008)

1.2 Parasite infections In contrast to commensalism, mutualism, phoresia, and symbiosis, which describe apathogenic ways of coexistence between organisms of different species, parasitism describes a relationship that is harmful to one of the partners. Parasites are defined as “organisms that live on and draw nutrients from another organism (the host), usually to the host’s detriment” (Nunn and Altizer, 2006). Given this definition, parasites can be found within the taxonomic groups of protozoa, metazoa, viruses, bacteria and fungi. The field of classical parasitology, however, exclusively concerns eukaryotic unicellular (protozoa) and multicellular (helminths and arthropods) pathogens (Hiepe et al., 2006). In this thesis, the term “parasite” will also only refer to eukaryotic organisms. The most common parasite classification is the differentiation between ecto- and endoparasites. Ectoparasites do not invade their host´s bodies but are limited to the body surface. Arthropods like ticks, fleas and lice are typical examples. Parasites that live inside their host are known as endoparasites. Some species colonize specific organs, such as the gastrointestinal tract (e.g. strongylid and ascarid nematodes, cestodes and protozoa like Giardia spp.), the liver (e.g. liver flukes), lungs (e.g. metastrongylid nematodes) or kidneys (e.g. nematodes like Dioctophyme renale and trematodes like Schistosoma spp). Hemoparasites live either in the blood fluid (e.g. nematode microfilaria or protozoa like Trypanosoma spp.) or within the blood cells (e.g. protozoa like Plasmodium spp. and Babesia spp.) (Hiepe et al., 2006). A further differentiation, particularly applicable to ectoparasites, bases on the duration of the contact between host and parasite. Temporary parasites remain only for a short time on the host and develop and reproduce in the environment (e.g. ticks), while stationary parasites (e.g. lice) are permanently host-dependent and develop and reproduce on or in its body (Deplazes et al., 2012). Distinctions can be made between obligate parasites (e.g. sucking lice, cestodes), 5 which are absolutely dependent on a host, and facultative parasites (e.g. some Laelaptidae mites), which are only occasionally parasitic. Furthermore, periodic parasites (e.g. Trombiculidae mites), of which only certain developmental stages live parasitic are to be distinguished from permanent parasites which live parasitic throughout all developmental stages (e.g. sucking lice) (Deplazes et al., 2012; Hiepe et al., 2006; Maaz, 2018). Moreover, parasites might differ in their host specificity: monoxenous parasites (e.g. most sucking lice) are restricted in their infection ability to a single host species, while oligoxenous parasites (e.g. ruminant trichostrongyles) are able to infect a few and polyxenous parasites (e.g. Trombiculidae mites) a large number of different host species. In general, parasite life cycles exhibit varying levels of complexity. Homoxenous parasites need only one host to complete their cycle. Among these, some species undergo a free-living development in the environment before being infective for a host (e.g. strongylid nematodes). The development of heteroxenous parasites (e.g. cestodes and trematodes) requires one or more intermediate hosts before infection of the definitive hosts, in which parasite reproduction occurs, is possible (Hiepe et al., 2006). The lancet liver fluke (Dicrocoelium dendriticum), for instance, passes a snail and an ant during its development to be able to infect the ruminant definitive host (Tarry, 1969). Intermediate hosts can also act as vectors, carrying the parasite from one host to another and hence promote its distribution and transmission. Vectors are particularly relevant for hemoparasites, which are transmitted by arthropods like fleas, lice, ticks, mosquitoes, blackflies and midges (Klein et al., 2019; Sehgal, 2015; Shelley and Coscarón, 2001). Per definition, parasite infections are detrimental for the host. Those negative impacts can be direct or indirect. Tissue damage due to parasite attachment (e.g. cestodes), expansion or migration (e.g. ascarid nematodes) and the loss of blood or lymphoid fluids connected to these damages or by parasite feeding (e.g. hematophagous strongylid nematodes and blood sucking arthropods) are direct impacts (Deplazes et al., 2012; Hiepe et al., 2006; Klein, 2019; Springer, 2015). By withdrawal of nutrients (e.g. ascarid nematodes) or the production of toxic or immunologically active substances (e.g. Trypanosoma spp., Plasmodium spp.), parasites can also affect their host indirectly (Bush et al., 2001; Klein, 2019). The hosts, in contrast, react with specific immune responses, the development of resistances (Hess and Edwards, 2002; Hoste et al., 2005; Tschirren et al., 2007) and behavioral avoidance and removal strategies (Friant et al., 2016; Grear et al., 2013; Poirotte and Kappeler, 2019). Over evolutionary timescales, this coevolution of hosts and parasites represent a race of arms (Anderson, 2000; Klein, 2019; Mccoy, 2009; Springer, 2015). Parasite infections are hence a driving force for many life history adaptations (Cable and van Oosterhout, 2007; Fredensborg

6 and Poulin, 2006; May and Anderson, 1983) and are in this way firmly embedded in many ecological interactions which will be briefly introduced in the next subchapter (Hudson et al., 2006; Marcogliese, 2004).

1.3 Relationships between parasites, hosts and ecosystems Although parasites represent more than 40% of the biodiversity worldwide (Bordes and Morand, 2009; Dobson et al., 2008; Gómez and Nichols, 2013; Weinstein and Kuris, 2016), parasitic species have been almost completely neglected in the context of environmental changes by HF (Bonneaud et al., 2009; Gillespie and Chapman, 2006; Vaz et al., 2007). Parasitism is regarded as the worldwide most successful lifestyle (Hechinger and Lafferty, 2005; Price, 1980; Thompson, 1994; Weinstein and Kuris, 2016) and the number of parasites infecting vertebrates alone is estimated to exceed the number of their host species by a multiple (Poulin and Morand, 2000). Parasites regulate their host´s population dynamics and community structure and perform important functions in food webs by impacting nutrient flow via predation and herbivory (Dunne et al., 2013; Lafferty et al., 2007, 2006; Marcogliese, 2004; Mouritsen and Poulin, 2005; Thomas et al., 1999; Valladares et al., 2012). While the vital role of parasites in ecological processes is gaining increasing recognition, results on their response to present environmental changes are ambiguous. A few studies relate parasite prevalences to environmental changes in terrestrial ecosystems, but their results have not revealed a clear pattern. Several studies observed higher infection levels of ectoparasites (Allan et al., 2003; Froeschke et al., 2013; Junge et al., 2011; Ogrzewalska et al., 2011; Schwitzer et al., 2010), gastrointestinal parasites (Chapman et al., 2006; Ferrari et al., 2015; Froeschke et al., 2013; Gillespie et al., 2005; Gillespie and Chapman, 2008, 2006; Klaus et al., 2018; Mbora and McPeek, 2009; Schwitzer et al., 2010; Trejo-Macías et al., 2007) and hemoparasites (Fornberg, 2017; Ogrzewalska et al., 2011; Perez-Rodriguez et al., 2018; Vaz et al., 2007) in hosts from fragmented and degraded habitats. Other studies found the opposite result (ectoparasites: Bolívar-Cimé et al., 2018; Bush et al., 2013; gastrointestinal parasites: Bordes et al., 2015; Gay et al., 2014; Martínez-Mota et al., 2018; Resasco et al., 2019; Taylor & Merriam, 1996; Vandergast & Roderick, 2003; hemoparasites: Bonneaud et al., 2009; Chasar et al., 2009; Cottontail et al., 2009). Additionally, equivocal findings (Raharivololona and Ganzhorn, 2009; Tchoumbou et al., 2020; Valdespino et al., 2010) or the absence of habitat influences on parasite infections (De Aguilar et al., 2018; Navarro- Gonzalez et al., 2010) were reported. 7

Elevated levels of parasitism in fragmented and degraded habitats were mostly explained by restricted migration rates leading to higher host density (Allan et al., 2003; Fornberg, 2017; Froeschke et al., 2013; Mbora and McPeek, 2009; Trejo-Macías et al., 2007; Vaz et al., 2007) and social group size (Gabriel et al., 2018; Ogrzewalska et al., 2011). Resulting higher rates of interaction between animals were suggested to promote parasite transmission. Also, increased host susceptibility to parasite infections by compromised immune function due to lower food quality, reduced availability of resources and higher levels of stress in fragmented habitats were suggested (Chapman et al., 2006; Gabriel et al., 2018; Irwin et al., 2010; Junge et al., 2011; Schwitzer et al., 2010). In addition, increasing temperature in fragmented areas was suspected to foster parasite, but also vector development, particularly relevant for vector borne blood parasites (Perez-Rodriguez et al., 2018; Sehgal, 2015). In contrast, reduced levels of parasitism in fragmented and degraded habitats were explained by effects of HF impairing parasite (Martínez-Mota et al., 2018; Vandergast and Roderick, 2003) and vector (Bordes et al., 2015; Chasar et al., 2009; Cottontail et al., 2009) survival and reproduction. Impeded parasite transmission via changed host-parasite interactions (Bordes et al., 2015; Taylor and Merriam, 1996) and local parasite extinction with missing recolonization (Bush et al., 2013; Resasco et al., 2019) were also assumed as causes for lower parasite prevalences in fragmented and degraded environments. It is likely that differences in host biology, parasite communities, parasite life cycles, as well as habitat type and composition may explain most of these contradicting results. The finding of a universal answer to whether HF leads to an increase or decrease in parasitic infections may therefore be impossible. Nevertheless, more detailed investigations of individual factors influencing parasites in altered ecosystems are still lacking but needed to fill this overall lack of knowledge. By differentiating individual host- and habitat-related factors using generalized linear mixed modeling, this thesis will contribute to this ongoing debate for four host taxa, two lemur species and two rodent species.

1.4 Biodiversity, habitat loss and fragmentation in Madagascar The island of Madagascar in the Indian Ocean is located south of the equator and at a distance of around 500 km to the east coast of continental Africa. With an area of 587,000 km2 (Donque, 1972), it is the fourth-largest island in the world. Central highlands stretch in north- south direction and divide the island into two main climatic zones (Donque, 1972). As humid trade winds from the North-East deliver rains on the eastern flanks of the central plateau, eastern Madagascar is characterized by a humid climate and rainfall throughout the year,

8 allowing the growth of evergreen rainforest. With dry deciduous forest landscapes in northwestern to western Madagascar and arid spiny forests at the southern tip of the island, the west of the island is generally dryer and rainfall is highly seasonal. For example, while rain is almost completely lacking in the dry season from May to October, a humid and hot rainy season lasts from November to April in northwestern Madagascar. The variety of different bio-climatic zones across Madagascar in combination with a long lasting isolation of the island enabled the development of a particularly rich and unique biodiversity (Ali and Huber, 2010; Brown et al., 2016; Goodman and Benstead, 2005). Over 90% of the approximately 12,000 vascular plants on Madagascar are endemic (Schatz et al., 2000). The more than 700 Malagasy vertebrate species also show high rates of endemism: about 50% of the birds and even more than 98% of the reptile, amphibian and mammal species are exclusively found on the island (Brown et al., 2016; Ganzhorn et al., 2001; Langrand and Willmé, 1997). At the same time, Madagascar´s human population is subject to strong growth. Estimates about the time of human arrival on the island vary between 2,000-10,000 before present (Douglass et al., 2019; Tollenaere et al., 2010). By 2019, the Malagasy human population reached a number of almost 27 million people. Still, the population is expected to grow to more than 50 million by the year 2050 (United Nations, 2019). This development is linked to severe human-wildlife conflicts that need to be solved to reconcile the urgency of nature conservation with the necessity to achieve food security (Molotoks et al., 2017). Conflicts become visible through the continuing loss of natural vegetation: in the years from 1953 to 2014 alone, the forest cover of Madagascar was reduced by 44% (Vieilledent et al., 2018). Residual forests are highly fragmented (Harper et al., 2007) and 46% of the forest is located closer than 100 m to a forest edge (Vieilledent et al., 2018). Since more than 90% of Malagasy species are considered to live exclusively in forests and woodlands, this development is alarming (Dufils, 2003). Facts, such as that more than 94% of the lemurs species in Madagascar are threatened by extinction, show an urgent need for intervention (Schwitzer et al., 2014). Hence, high rates of endemism, species diversity and expansion of human activities in parallel make Madagascar a global priority region for conservation action (Estrada et al., 2018; Myers et al., 2000; Schwitzer et al., 2014).

1.5 Parasites of lemurs and rodents in Madagascar Lemurs form a very diverse endemic clade of Malagasy mammals with more than 100 species belonging to 15 genera (Estrada et al., 2018; Schwitzer et al., 2014). They are the best studied group of the island´s fauna, but knowledge on their parasites is still small compared to other 9 primate taxa (Ezenwa et al., 2017). Intense research on lemur parasite taxonomy was performed between 1950 and 1980 and was based on detailed morphological descriptions. Regarding gastrointestinal parasites, substantial work was conducted by Alain Chabaud, Edouard Brygoo and Annie Petter (Irwin and Raharison, 2009). In terms of lemur ectoparasites, much fundamental work was realized by Harry Hoogstraal on Acari (summarized in Klein, 2019) and by Ronald A. Ward on sucking lice (summarized in Durden et al., 2010). This taxonomic work continued well into the recent past, when new species descriptions became available for several lemur ectoparasite species (ticks: Blanco et al., 2013; Klein et al., 2018, mites: Bochkov et al., 2010; Stekolnikov et al., 2019b; Stekolnikov & Fain, 2004, lice: Durden et al., 2010, 2017, 2018), gastrointestinal parasite species (pinworms: (Del Rosario Robles et al., 2010; Hugot et al., 1995; Hugot and del Robles, 2011), and hemoparasites (protozoa: Larsen et al., 2016, microfilaria: Klein et al., 2019). However, although the importance of genetic sequence data for the clarification of taxonomic questions is increasingly recognized, DNA sequences are still not available for all taxa. The endemic rodents of Madagascar encompass 27 species subdivided into nine genera within the rodent subfamily of Nesomyinae (Muridae) (Musser and Carleton, 2005). Compared to lemurs, little is known about the parasites of endemic Malagasy rodents (Morand and Krasnov, 2007). Apart from three publications on taxonomy of strongylid nematodes in Malagasy Muridae (Durette-Desset et al., 2014, 2007, 2002), the gastrointestinal parasites of the subfamily Nesomyinae have only been considered by Raharivololona et al. (2007) surveying parasites in fecal samples of Eliurus webbi from southern Madagascar. In terms of ectoparasites, the tick Haemaphysalis nesomys infesting red forest rats (Nesomys rufus) has been described by Hoogstraal et al. (1966) in the course of early lemur ectoparasite descriptions. Additionally, mesostigmatic mites have been reported to infest Nesomyinae in their nests (Dowling, 2006). Specific hemoparasites of endemic Malagasy rodents are so far not known. Recent studies on parasites of Malagasy mammals also included invasive rodents in their set of investigated host species. Three introduced rodents are reported to occur in Madagascar: the black rat (Rattus rattus), the brown rat (R. norvegicus) and the house mouse (Mus musculus) (Miljutin and Lehtonen, 2008). Most of the parasite species found on invasive rodents are co-invasive and were brought with them during colonization (Ehlers et al., 2019; Laakkonen et al., 2003a; Pratt and Karp, 2006). For example, the gastrointestinal parasite morphotypes found in black rats by Raharivololona et al. (2007) were most likely introduced and not native to Madagascar. Another study on Cryptosporidium spp. and Giardia spp.

10 infections in livestock, humans and wildlife in eastern Madagascar, reported the presence of both parasite genera in black rats and humans, while lemurs (Propithecus diadema and Hapalemur griseus) remained uninfected (Spencer and Irwin, 2020). In terms of ectoparasites, the oriental rat flea (Xenopsylla cheopis) can be found on all mentioned invasive rodents. The flea is known to be involved in the spread of the zoonotic bacterium Yersinia pestis, the causative agent of plague (Chanteau et al., 1998; Ehlers et al., 2020; Tollenaere et al., 2010). Finally, also co-invasive hemoparasites of the species Trypanosoma lewisi were detected in black rats in rainforests of the Ranomafana National Park in south-eastern Madagascar (Laakkonen et al., 2003b). Due to climate change and increasing human activities within formerly remote areas, a general increase of foreign parasite infections in Malagasy wildlife can be expected (Barrett et al., 2013). The trend is already visible today: introduced Trypanosoma sp. hemoparasites have been detected in the endemic Nesomys rufus from south eastern Madagascar (Laakkonen et al., 2003b) and infections with the zoonotic protozoa Cryptosporidium sp. were reported in greater bamboo lemurs (Prolemur simus) and brown mouse lemurs (Microcebus rufus) from eastern Madagascar (Rasambainarivo et al., 2013). Moreover, the canine heartworm (Dirofilaria immitis) was detected in a brown mouse lemur (Microcebus rufus) from eastern Madagascar, which was associated to a generally increasing abundance of domestic dogs in the area (Zohdy et al., 2019). Anthropogenic disturbance is, however, reported to also promote infections with native parasites: human presence was related to an increasing parasite diversity in Indris (Indri indri) from eastern (Junge et al. (2011) and ring-tailed lemurs from southern Madagascar (Loudon and Sauther, 2013). In addition to human presence, habitat condition was related to parasite infections of Malagasy mammals. Pinworm prevalences in blue-eyed black lemurs (Eulemur flavifrons) were reported to be higher in degraded secondary habitats than in primary forests. Rakotoniaina et al. (2016), however, did not find a relationship between habitat disturbance and gastrointestinal parasite infections of gray mouse lemurs (M. murinus) and fat-tailed dwarf lemurs (Cheirogaleus medius) in western Madagascar, and also Ehlers et al. (2019) could not find impacts of habitat degradation on ectoparasites infestations of various endemic, introduced and domestic mammalian hosts in the south of the island. The findings of Raharivololona & Ganzhorn (2009) were ambiguous: excretion of gastrointestinal parasite eggs and oocysts by gray mouse lemurs from southern Madagascar differed between four investigated habitat fragments with different quality of forest. Animals from degraded habitats 11 exhibited an elevated egg excretion of ascarid nematodes and tapeworms, while the opposite was found for eggs of Subulura nematodes and protozoan oocysts. Most work on environmental impacts on parasites of Malagasy wildlife focused on aspects of habitat degradation and human presence. However, most studies considered only a low spatial scale, low numbers of investigated host individuals, few host species and a narrow spectrum of parasite species. Moreover, single factors in the extensive field of anthropogenic environmental change like habitat size and edge effects have not been considered in detail or in a differentiated manner. This work will hence contribute new information on parasite infections in a changing environment by providing a new, large dataset of ecto- and gastrointestinal infections in four different host species living along gradients of edge effects, vegetation structure and fragmentation.

1.6 Introduction of the studied host species including some notes on their parasites The four investigated host species (Figure 1.1) are the most abundant mammals in the fragmented dry forests in northwestern Madagascar (Ito et al., 2013). The two primate species, the gray mouse lemur (Microcebus murinus, ~ 54 g) and the golden-brown mouse lemur (M. ravelobensis, ~ 56 g), and the two rodent species, the endemic western tuft-tailed rat (Eliurus myoxinus, ~ 66 g) and the invasive black rat (Rattus rattus, ~ 100 g) are similar in their nocturnal activity, their habit of spending the day in sheltered sleeping sites, their arboreal lifestyle and their occurrence in high population densities.

Figure 1.1: Gray mouse lemur (Microcebus murinus) (a), golden-brown mouse lemur (M. ravelobensis) (b), western tuft-tailed rat (Eliurus myoxinus) (c) and black rat (Rattus rattus) (d) with their respective distribution areas (IUCN Red List, 2020)

Although the gray mouse lemur and the golden-brown mouse lemur occur in sympatry in the studied area, the distribution of M. murinus is much larger than that of M. ravelobensis (Figure 1.1). M. murinus occurs all along the Malagasy west coast up to the river Sofia in the Northwest and is listed by the IUCN under least concern (IUCN Red List, 2020; Mittermeier, 2010; Olivieri et al., 2007; Pastorini et al., 2001; Yoder et al., 2002). In contrast, M. ravelobensis is limited to the inter-river-system between the rivers Betsiboka and Mahajamba and is classified as vulnerable (IUCN Red List, 2020; Olivieri et al., 2007). M. murinus can be also found in degraded and small habitat fragments while M. ravelobensis shows a lower resilience to environmental changes and is restricted to larger patches of less degraded habitats (Andriatsitohaina et al., 2020b). Individuals of both mouse lemur species forage solitarily during the night, while they sleep in groups in sheltered sleeping sites during the day. M. murinus depends on wooden tree holes as sleeping sites (Radespiel et al., 2003). M. ravelobensis is not highly dependent in tree holes and sometimes sleeps in self-built leaf nests (Radespiel et al., 2003; Thorén et al., 2010). Reproduction of both species is well adapted to the seasonal climate. After mating season starts in the end of August, the first of two possible litters is born at the beginning of the rainy season (Rina Evasoa et al., 2018; Schmelting et al., 2000; Weidt et al., 2004). The omnivorous diet of both species encompasses insects, insect secretions, fruits, gum and nectar (Thorén et al., 2016). However, diet composition varies between the two species, since M. murinus can be classified as a seasonal dietary generalist (Radespiel, 2016) and M. ravelobensis is considered to feed on a less diverse diet across seasons (Radespiel, 2016). Further differences between these two species have been identified particularly in aspects of social structure. Females of M. murinus are generally dominant over males (Devinney et al., 2001; Radespiel et al., 1998), while M. ravelobensis shows no distinct female dominance (Eichmueller et al., 2013). Also sleeping group composition differs, as M. murinus sleeps divided by sexes and M. ravelobensis also forms mixed-sex sleeping groups (Radespiel et al., 1998; Weidt et al., 2004). Home ranges in size of about 2 ha overlap between individuals and are reported for males, at least in the case of M. murinus, to increase in the mating season (Radespiel, 2000; Radespiel et al., 2001; Weidt et al., 2004). The knowledge about the parasite fauna of M. murinus is more extensive than that of M. ravelobensis. In terms of ectoparasites, both species are known to harbor ticks (Haemaphysalis microcebi), sucking lice (Lemurpediculus spp.) and mites (Laelaptidae, Trombiculidae) (Durden et al., 2021, 2018; Klein et al., 2018; Stekolnikov et al., 2019; Zohdy and Durden, 2016). For M. murinus, also infestations with atopomelid and chortoglyphid mites as well as other species of haemaphysaline ticks were reported (Zohdy and Durden, 13

2016). Only one study focused on gastrointestinal parasites of M. ravelobensis and reported the presence of ascarid and oxyurid nematodes as well as cyclophyllid cestodes (Radespiel et al., 2015). The repertoire of gastrointestinal parasites of M. murinus encompasses infections with nematodes (Rhabditida, Strongylida, Oxyurida, Ascaridida, Spirurida and Enoplida), cyclophyllid cestodes, dicrocoeliid trematodes and protozoa (eimeriid coccidia) (Hugot et al., 1995; Irwin and Raharison, 2009; Kessler et al., 2016; Radespiel et al., 2015; Raharivololona, 2009, 2006; Raharivololona et al., 2007; Springer and Kappeler, 2016). Onchocercid microfilaria are the only hemoparasites confirmed for both mouse lemur species so far (Irwin and Raharison, 2009; Klein et al., 2019). Besides studies mentioned in the previous subchapter, which investigate parasite infections of gray mouse lemurs in relation to habitat degradation (Raharivololona and Ganzhorn, 2009; Rakotoniaina et al., 2016), parasite infections were also discussed in the context of season: prevalences of ticks and sucking lice increased in gray and golden brown mouse lemurs in the course of the dry season (Klein et al., 2018) and excretion of helminth eggs in M. murinus was highest in the hot rainy season (Raharivololona and Ganzhorn, 2010). Host-related aspects like sex and body condition where found to have no influence on ectoparasite prevalences in both mouse lemur species (Klein et al., 2018). Male M. murinus were however found to develop higher tapeworm prevalences with age (Hämäläinen et al., 2015). In addition, several studies relating genetic MHC diversity of gray mouse lemurs to gastrointestinal parasite infections, found a positive relationship between specific alleles and parasite load (Schad et al., 2005; Schwensow et al., 2010). The western tuft-tailed rat is one of 12 other species within the genus Eliurus. Occurring from Ambovombe in the south to Antsiranana at the northernmost tip of Madagascar, the distribution area is large and encompasses the entire western half of the island (Figure 1.1) (Goodman, 2016). The species depends on spiny and dry deciduous forest habitats but can also be found in degraded areas (Randrianjafy et al., 2008). However, Andriatsitohaina et al. (2020b) found a high susceptibility to HF. Literature on home range size and vagility of western tuft-tailed rats is not available. However, the animals are known to live solitarily and spend the days sleeping in tree holes or dens in the ground (Carleton, 1994; Goodman, 2016). E. myoxinus has a promiscuous mating system and raises relatively small litters of around three juveniles (Goodman, 2016). Seasonality in reproduction is suspected towards the end of the dry season, but supporting information is not available (Randrianjafy et al., 2008). The herbi- or frugivorous diet consists of seeds, fruits and other parts of plants (Carleton, 1994; Ramanamanjato and Ganzhorn, 2001; Randrianjafy, 2003; Randrianjafy et al., 2008; Shi et

14 al., 2013). Until now, parasite infections of the western tuft-tailed rat have not been investigated. The black rat (Rattus rattus) is one of three invasive rodents on Madagascar, but the only one that thrives in various natural habitats throughout the island (Figure 1.1), and can be nowadays found even in remote areas and pristine forests (Goodman, 1995). Black rats were introduced to Madagascar approximately 3000-10,000 years ago following human colonization from Asia (Tollenaere et al., 2010). Although a competition for resources between black rats and native species has often been suspected, a displacement of a native species by the invasive rats has yet not been clearly demonstrated (Andriatsitohaina et al., 2020b; Miljutin and Lehtonen, 2008; Ramanamanjato and Ganzhorn, 2001). Black rats spend periods of inactivity in self-built nests, flexible in material and exposed or in already available cavities (Münster, 2003). The omnivorous diet includes seeds, fruits and invertebrates (Clark, 1982). As black rats can live alone or in larger groups of up to fifty individuals, sociality and group composition is flexible (Münster, 2003). Females can produce up to five litters of 6-12 juveniles per year while reproduction is not seasonal but restricted to the availability of resources (Corbet and Southern, 1977). The cosmopolitan rodent is noted to harbor a large variety of enteral, ecto- and hemoparasites. Subpopulations worldwide show a simultaneous presence of many different endo- and ectoparasite species in high prevalences (Claveria et al., 2005; Mafiana et al., 1997; Pakdel et al., 2013; Singla et al., 2008; Siti Shafiyyah et al., 2012). Within Madagascar, fecal sample analysis of a southern black rat subpopulation detected infections with ascarid, strongylid, trichurid, oxyurid and spirurid nematodes, cyclophyllid cestodes and eimeriid coccidia (Raharivololona et al., 2007). In terms of ectoparasites, ticks, sucking lice and fleas were reported to infest R. rattus in Madagascar (Ehlers et al., 2019; Hastriter and Dick, 2009; Kim and Emerson, 1974; Uilenberg et al., 1979). Since most of the parasite species found in and on black rats in Madagascar are also known from black rats in other parts of the world, it is suspected that Rattus rattus, as an invasive species, can potentially spread non-endemic parasites to native Malagasy wildlife (Smith and Carpenter, 2006). Although known from other parts of the world, such cases in Madagascar have not been reported yet (Morand et al., 2015). The high number of similarities in the biology of the four investigated taxa suggest overall similar patterns of parasite infections. Those are hence assumed to be impacted by HF in similar ways. However, it is unclear whether this also applies to the invasive R. rattus, as the high adaptability of this species to changing environmental factors might also provide 15 different conditions for parasitic infections. Details are, however, not known, so this thesis shall contribute new information to this aspect.

1.7 Aims of the study The present work aims to investigate the understudied impacts of forest fragmentation on ectoparasites and gastrointestinal parasites in four small mammalian host species in northwestern Madagascar. The investigations were conducted in two fragmented dry forest networks in the Malagasy Boeny Region (Ankarafantsika National Park [ANK], Mariarano Classified Forest [MAR]). The study areas offered both large intact forests and forest fragments with a high variation in size, shape, distance to edges and vegetation structure to test potential influences of those factors on parasite infections. Fragments have been stable in shape and size over at least several decades and the surrounding matrix (savannah) is highly contrasting to the dry deciduous forest fragments, providing an adequate setting to test for edge effects on parasites. In addition, the study areas are inhabited by all four chosen model hosts. The two mouse lemur species (M. murinus and M. ravelobensis) and two rodent species (E. myoxinus and R. rattus), could be captured und sampled in relatively high numbers, securing a sufficient dataset. It allowed the comparison of distantly related (primates vs. rodents) as well as closely related hosts (M. murinus vs. M. ravelobensis), the comparison of hosts with different dietary requirements (omnivorous vs. frugivorous), social structures (gregarious vs. solitary) and the comparison of endemic hosts (mouse lemurs, E. myoxinus) with an invasive host species (R. rattus). Previous studies demonstrated the presence of ecto-, gastrointestinal and hemoparasites in communities of M. murinus and M. ravelobensis in the Ankarafantsika National Park (Klein, 2019; Klein et al., 2019, 2018; Radespiel et al., 2015). Temporary as well as stationary, and homoxenous as well as heteroxenous parasite species were previously detected, providing the opportunity to study the impact of such life cycle traits on the response to fragmentation. According to fundamental differences in biology and detection of ecto- and gastrointestinal parasites, this thesis is subdivided into two chapters (chapter II and III) examining environmental impacts on each parasite category separately. Due to reduced availability of resources for the host, which might lead to a reduced immune function, and crowding effects caused by limited migration options for hosts in fragments facilitating pathogen transmissions, rates of parasitism were anticipated to increase in fragmented, degraded and edge habitats. In particular, stationary and homoxenous parasites like lice and pinworms were expected to occur in higher prevalences in hosts from forest edges and degraded habitat fragments compared to hosts from interior, pristine and

16 continuous habitats. According to this, hosts from populations with higher densities and with low body mass were expected to exhibit higher prevalences of stationary and homoxenous parasites. Since temporary and heteroxenous parasites like ticks and cestodes might themselves be negatively affected by altered abiotic environmental conditions in degraded and fragmented habitats, effects increasing host susceptibility for those parasites were expected to appear smaller. Overall, the negative environmental effects on parasites were expected to be weaker for gastrointestinal endoparasites than for ectoparasites, since gastrointestinal endoparasites parasites might be more protected from environmental influences. 17

2 Publications 2.1 Forest edges affect ectoparasite infestation patterns of small mammalian hosts in fragmented forests in Madagascar

Frederik Kienea,b, Bertrand Andriatsitohainab,c, Malcolm S. Ramsayb,d, Herinjatovo Rakotondramananae, Romule Rakotondravonyc,e, Ute Radespielb, Christina Strubea (2020)

Published in the International Journal for Parasitology 2020; 50: 299-313 doi: 10.1016/j.ijpara.2020.01.008 a Institute for Parasitology, Centre for Infection Medicine, University of Veterinary Medicine Hannover, Buenteweg 17, 30559 Hanover, Germany b Institute of Zoology, University of Veterinary Medicine Hannover, Buenteweg 17, 30559 Hanover, Germany c Ecole Doctorale sur les Ecosystèmes Naturels (EDEN), University of Mahajanga, 5 Rue Georges V - Immeuble KAKAL, Mahajanga Be, B.P. 652, Mahajanga 401, Madagascar d Department of Anthropology, University of Toronto, 19 Russell Street, Toronto, ON M5S 2S2, Canada e Faculté des Sciences, de Technologies et de l’Environnement, University of Mahajanga, 5 Rue Georges V - Immeuble KAKAL, Mahajanga Be, B.P. 652. Mahajanga 401, Madagascar

Abstract: Habitat loss and fragmentation drive the worldwide depletion of biodiversity. Although it is known that anthropogenic disturbances severely affect host and ecosystem integrity, effects on parasites are largely understudied. This study aims to investigate if and how habitat fragmentation affects the composition of ectoparasite communities on small mammalian hosts in two networks of dry deciduous forest fragments in northwestern Madagascar. Forest sites differing in size, proportion of edge habitat and host density were studied in the Ankarafantsika National Park and in the Mahamavo region. A total of 924 individuals of two mouse lemur species, Microcebus murinus (n=200) and Microcebus ravelobensis (n=426), and two rodent species, endemic Eliurus myoxinus (n=114) and introduced Rattus rattus (n=184), were captured to assess ectoparasite infestations. Ectoparasite prevalence and ectoparasite species richness (EPSR) were statistically related to nine ecological variables applying generalized linear mixed models. Hosts harbored ticks (Haemaphysalis microcebi),

18 mites (Schoutedenichia microcebi, Listrophoroides spp., Laelaptidae gen. spp.) and sucking lice (Lemurpediculus spp., Polyplax sp., Hoplopleuridae gen. sp.). Parasite prevalence differed significantly between host species for all detected parasite taxa. Proximity to the forest edge led to a significant reduction of ectoparasites. Parasite-specific edge effects were observed up to a distance of 750 m to the forest edge. The obtained results imply that habitat fragmentation impacts ectoparasite communities, in particular by negatively affecting temporary parasite species. The results are best explained by an interplay of parasite life cycles, responses to changes in abiotic factors induced by edges and host-specific responses to habitat fragmentation. The negative responses of most studied ectoparasite taxa to forest edges and habitat fragmentation demonstrate their ecological vulnerability that may eventually threaten the integrity of ecosystems and potentially impact ectoparasite biodiversity worldwide.

Key words: habitat fragmentation, lemurs, rodents, ticks, mites, lice

Author contributions: Concept and study design: Ute Radespiel, Christina Strube Sampling: Frederik Kiene Data analyses: Frederik Kiene Discussion and consultation: Frederik Kiene, Bertrand Andriatsitohaina, Malcolm S. Ramsay, Herinjatovo Rakotondramanana, Ute Radespiel, Christina Strube Manuscript: Frederik Kiene, Ute Radespiel, Christina Strube 19

2.2 Habitat fragmentation and vegetation structure impact gastrointestinal parasites of small mammalian hosts in Madagascar

Frederik Kienea,b, Bertrand Andriatsitohainaa,c, Malcolm S. Ramsaya,d, Romule Rakotondravonyc,e, Christina Strubeb, Ute Radespiela

Published in Ecology and Evolution 2021; 00: 1-23 doi: 10.1002/ece3.7526 a Institute of Zoology, University of Veterinary Medicine Hannover, Buenteweg 17, 30559 Hanover, Germany b Institute for Parasitology, Centre for Infection Medicine, University of Veterinary Medicine Hannover, Buenteweg 17, 30559 Hanover, Germany c Ecole Doctorale Ecosystèmes Naturels (EDEN), University of Mahajanga, 5 Rue Georges V - Immeuble KAKAL, Mahajanga Be, B.P. 652, Mahajanga 401, Madagascar d Department of Anthropology, University of Toronto, 19 Russell Street, Toronto, ON M5S 2S2, Canada e Faculté des Sciences, de Technologies et de l’Environnement, University of Mahajanga, 5 Rue Georges V - Immeuble KAKAL, Mahajanga Be, B.P. 652. Mahajanga 401, Madagascar

Abstract Deleterious effects of habitat loss and fragmentation on biodiversity have been demonstrated in numerous taxa. Although parasites represent a large part of worldwide biodiversity, they are mostly neglected in this context. We investigated the effects of various anthropogenic environmental changes on gastrointestinal parasite infections in four small mammal hosts inhabiting two landscapes of fragmented dry forest in northwestern Madagascar. Coproscopical examinations were performed on 1,418 fecal samples from 903 individuals of two mouse lemur species, Microcebus murinus (n = 199) and M. ravelobensis (n = 421), and two rodent species, the native Eliurus myoxinus (n = 102) and the invasive Rattus rattus (n = 181). Overall, sixteen parasite morphotypes were detected and significant prevalence differences between host species regarding the most common five parasites may be explained by parasite host specificity or host behavior, diet and socioecology. Ten host- and habitat- related ecological variables were evaluated by generalized linear mixed modeling for significant impacts on the prevalence of the most abundant gastrointestinal parasites and on

20 gastrointestinal parasite species richness (GPSR). Forest maturation affected homoxenous parasites (direct life cycle) by increasing Lemuricola, but decreasing Enterobiinae gen. sp. prevalence, while habitat fragmentation and vegetation clearance negatively affected the prevalence of parasites with heterogonic environmental (i.e., Strongyloides spp.) or heteroxenous (indirect cycle with intermediate host) cycles, and consequently reduced GPSR. Forest edges and forest degradation likely change abiotic conditions which may reduce habitat suitability for soil-transmitted helminths or required intermediate hosts. The fragility of complex parasite life cycles suggests understudied and potentially severe effects of decreasing habitat quality by fragmentation and degradation on hidden ecological networks that involve parasites. Since parasites can provide indispensable ecological services and ensure stability of ecosystems by modulating animal population dynamics and nutrient pathways, our study underlines the importance of habitat quality and integrity as key aspects of conservation.

Key words: habitat degradation, Microcebus, Eliurus, Rattus, edge effects, life cycle

Author contributions: Concept and study design: Christina Strube, Ute Radespiel Sampling: Frederik Kiene Data analyses: Frederik Kiene Discussion and consultation: Frederik Kiene, Bertrand Andriatsitohaina, Malcolm S. Ramsay, Christina Strube, Ute Radespiel Manuscript: Frederik Kiene, Christina Strube, Ute Radespiel 21

3 General discussion Parasites are core components of intact ecosystems (Hudson et al., 2006) and are well connected within species communities (Kuang and Zhang, 2011). By representing central junctions in food webs they act as mediators for the exchange of energy and nutrients between different trophic levels (Hatcher et al., 2012). By controlling their host´s population dynamics, parasites are important factors ensuring biodiversity and ecosystem stability (Marcogliese, 2004; Poulin, 2010). However, ecological modeling approaches studying the effects of habitat alterations on parasites are still scarce. While impacts on free-living organisms can be directly investigated by contextualizing the organism with its habitat, the understanding of parasite ecology requires a multi-layered approach. As a consequence of their life style and life cycle characteristics, parasites are exposed not only to the host (= host environment) but also to the environment surrounding the host (= external environment) (Hiepe et al., 2006). The relative impacts of host-related and environment-related factors on ectoparasite (chapter II) and gastrointestinal parasite infections (chapter III) were analysed in the two major chapters of this thesis for four host species that inhabit the fragmented forest landscapes of northwestern Madagascar. In order to integrate and evaluate the findings in a broader context, the following discussion is divided into three major parts that will discuss the impact of different parasite- related, host-related and habitat-related factors, respectively. The first part will discuss impacts of parasite life history and host specificity. Accurate predictions and conclusions about the effects of habitat alterations on the abundance of parasites are only possible if parasite life history traits are taken into account (Froeschke et al., 2013). Parasite host specificity is another key aspect for the understanding of infection patterns in different host species (Wells and Clark, 2019). Taken together, both aspects can be expected to be intricately linked to secure long-term persistence, successful development and reproduction (Dick and Patterson, 2007) of the different parasite types evaluated in the course of this work. The four investigated host species harbored five different ectoparasite types: ticks, mites of three different families (Trombiculidae, Laelaptidae, and Atopomelidae) and sucking lice. In terms of gastrointestinal parasites, sixteen different morphotypes could be distinguished, but low prevalences of 11 morphotypes precluded statistical modeling and they will therefore not be further evaluated in this context. The following discussion is therefore limited to the five most frequent morphotypes (Enterobiinae gen. sp., Lemuricola sp., Strongyloides spp., Subuluroidea fam. gen. spp. and spirurid egg1). Most important life history traits and notes on host specificity for the ten ecto- and gastrointestinal parasite types studied in more detail are summarized in Table 4.1.

In the second part of the discussion impacts of host-related aspects will be addressed. Since parasites depend heavily on their hosts and spend long periods or their entire lives on or in its body, the relationship between parasite and host is inevitably close. Hence, host-related aspects, i.e. the environment provided by the host, play one central role in the parasite´s ecology. Parasite infections can be, for example, influenced by the host´s behavior and diet, but also by its social structure and population density. They can also be associated to the sex and/or body condition of the host. The central objective of the present work was the identification of factors influencing parasite infections in an environment modified by habitat fragmentation, which will be discussed in the third part of the discussion. Impacts of six factors, used in the present work to characterize those influences on the investigated parasite types, will be considered. Two vegetation factors (vegetation clearance and forest maturation) are reflecting impacts of habitat condition/ degradation. The other four factors, directly connected to HF, are related to possible ecological edge effects (distance to the edge, percentage edge area) and the impact of habitat size (continuous forest vs. forest fragment, forest size).

Table 4.1: Overview on identified species within the investigated parasite types/morphotypes and notes on life cycle characteristics and host specificity. Mm = Microcebus murinus; Mr = M. ravelobensis; Em = Eliurus myoxinus; Rr = Rattus rattus parasite type host parasite species life cycle characteristics host specificity ectoparasites ticks Mm, Mr, Haemaphysalis microcebi obligate temporary-permanent parasites Ticks of the genus Haemaphysalis Em, Rr are typically oligo-polyxenous H. microcebi is reported to exhibit a three-host life cycle (Hoogstraal and Aeschlimann, extending over one generation per year (univoltinous). Blood 1982; Walker et al., 2003). meals are taken once each as larva and nymph (May-October) and as adult individual (November – April) (Klein, 2019). Hosts are infested by the ticks questing on exposed vegetation (Walker et al., 2003). Trombiculidae Mm, Mr, Schoutedenichia microcebi obligate temporary-periodic parasites Trombiculidae are generally mites Em, Rr known to feed on a wide range of Parasitic larvae infest their hosts, when those are in contact hosts, also including birds and with leaf litter and soil and feed once on lysed body tissue for a reptiles (polyxenous) (Morand few hours or days (temporary parasites). The larval stage is and Krasnov, 2007). followed by two nonfeeding and resting nymphal stages in the ground. The third nymphal stage and adult individuals live as arthropod predators in leaf litter and soil, where also eggs are deposited (Schöler, 2003).

Laelaptidae Mm, Mr Aetholaelaps trilyssa facultative or obligate temporary-periodic or -permanent nest Varying levels of host specificity mites Em not further identified associated parasites are described for parasitic mites Rr not further identified of this family. However, in a The life styles of different species within the family differ study on Laelaptidae infesting considerably, since free-living nonparasitic, facultative rodents in Brazil (Gettinger, parasitic and obligate ectoparasitic species are known (Kim, 1992), most species were reported 1985). Parasitic species feed on blood and other body fluids. to be restricted to only one host While some species are able to penetrate the host´s skin, others species (monoxenity). depend on preexisting wounds (Maaz, 2018). The mites exhibit five developmental stages: eggs, larvae, two nymphal stages and adults (Kim, 1985).

Atopomelidae Mm, Mr Listrophoroides sp. 1 obligate stationary-permanent parasites Species of the genus mites Em Listrophoroides sp. 2 Listrophoroides are Rr no infestations Although detailed information on life cycle, diet and monoxenous/oligoxenous epidemiology is not available, the mites can be suggested to parasites (Bochkov and OConnor, reproduce on the host, feed on epidermal detritus and are 2005). transmitted through direct physical contact (Baker, 2008; Bochkov et al., 2004; Bochkov and OConnor, 2006; Fain, 1981).

26 sucking lice Mm Lemurpediculus sp. 1 obligate stationary-permanent parasites Sucking lice are known to be Mr Lemurpediculus sp. 2 highly host specific Em Hoplopleura sp. (infestations After hatching from eggs that adhere to the hair of the host, (monoxenous) (Durden and with single lice in two cases) sucking lice develop through three larval stages to the adult Musser, 1994). Rr Polyplax sp. individual and are transmitted through direct body contact Hoplopleura sp. (Ehlers, 2020; Light et al., 2010).

gastrointestinal parasites

Oxyuridae Mm, Mr Enterobiinae gen. sp. homoxenous parasites Oxyuridae are typically restricted Lemuricola sp. to a small spectrum of hosts Em no infections Gravid females migrate to the host´s anus and deposit their (oligoxenous) (Hugot et al., 1996). Rr Enterobiinae gen. sp. eggs in the perianal region. The successive host picks up the Lemuricola sp. eggs directly from an infected animal or from contaminated materials in the environment. In the new host, larvae hatch (excretion of single eggs in within a few hours and quickly develop into adults (Taffs, one case each) 1976).

Strongyloides Mm, Mr, not further identified homoxenous parasites Most species of this genus are spp. Em, Rr known to be mono- or In addition to their parasitic homogonic cycle, where oligoxenous (Viney and Lok, parthenogenetic females in the gastrointestinal tract of their 2015). 27

hosts produce eggs which develop into an infective third stage larva in the environment, this nematodes can also undergo a heterogonic cycle. Here the environmental development of the third stage larvae is leading into a free-living generation involving sexual reproduction (Abadie, 1963; Streit, 2008). Most infections occur during contact with the soil, where third stage larvae penetrate the host´s skin and migrate via blood stream and lungs to its gastrointestinal tract. However, also direct oral infections, lactogenic infections from mother to offspring and perianal autoinfections are known for some species (Olsen et al., 2009).

Subuluroidea Mm, Mr not further identified heteroxenous parasites Host specificity, best explored for fam. gen. spp. Em not further identified the genus Subulura, is not very Rr not further identified Eggs are excreted along with the feces of the definitive host pronounced (oligo-polyxenous) and are ingested by arthropod intermediate hosts (mostly (Baker, 2008; Irwin and beetles and cockroaches). Hatched larvae migrate into the body Raharison, 2009). cavity of the arthropod and develop into infectious third-stage larvae. The definitive host is infected again by ingestion of the arthropod intermediate host (Irwin and Raharison, 2009; Quentin and Poinar, 1973).

Spiruromorpha Mm, Mr, not further identified heteroxenous parasites Host specificity is very variable (spirurid egg 1) Em among species. While P. muricola Rr Protospirura sp. Most of these are heteroxenous stomach parasites of birds and is infecting hosts of a wide range Gongylonema neoplasticum mammals which use insects like beetles and cockroaches as encompassing rodents, carnivores and primates (polyxenous) Spiruromorpha sp. 1 intermediate hosts (Montoliu et al., 2013). The definitive host (Smales et al., 2009), G. Spiruromorpha sp. 2 is again infected by ingestion of these arthropods (Schutgens et al., 2015). neoplasticum is restricted to hosts of the genus Rattus (oligoxenous) (da Costa Cordeiro et al., 2018; Setsuda et al., 2018).

3.1 Parasite life history and host specificity By taking the evolutionary step from a free-living existence to a parasitic life style, a future parasite has to solve multiple problems associated to transmission, invasion and survival within the host (Poulin and Randhawa, 2015). Heteroxenous parasites have developed complex life cycles, which involve multiple hosts for successful transmission by facilitating dispersal and extending the infective period (Pearson, 1972). To complete simple as well as more complicated life cycles, host-parasite interactions require adaptations of the parasite, which lead to different levels of host specificity (Blasco-Costa and Poulin, 2017; Strona et al., 2013; Wells and Clark, 2019). Homoxenous species like fur mites, sucking lice and several pinworms, which are mainly transmitted by direct physical contact, have mostly evolved high levels of host specificity (Fain, 1994; Hugot, 1999; Light et al., 2010). Since the frequency of intraspecies physical contact exceeds the frequency of interspecies contact in most host species, specialization provides an important advantage for the parasite (Clark and Clegg, 2017; Wells et al., 2019). In the context of coevolution, host specificity of homoxenous parasites might even lead to cospeciation of parasites in response to host speciation (Wells and Clark, 2019). Also in the present work, there is evidence for high levels of host specificity among the investigated mainly directly transmitted parasite types. Only the closely related mouse lemurs shared the same Atopomelidae mites (Listrophoroides sp.) and pinworm species (Enterobiinae gen. sp. and Lemuricola sp.), while the other hosts were not infected or harbored different species of the respective parasite types (e.g. different Listrophoroides sp. in E. myoxinus). Evidence for parasite cospeciation, which is commonly known for sucking lice (Light and Reed, 2009), is provided by M. murinus and M. ravelobensis being infested with different species of sucking lice from the genus Lemurpediculus (chapter II). Also nest-associated parasites often exhibit high rates of host specificity. Living in dens, burrows and nests, they have only access to a limited range of different hosts which visit these spots. According to this, three different species of Laelaptidae mites infesting each the mouse lemurs, E. myoxinus and R. rattus could be distinguished in this study. In contrast to the nest associated or even stationary (e.g. Ornithodoros lahorensis) soft ticks of the family Argasidae, which are often more or less host specific, hard ticks of the family Ixodidae are temporary parasites and often less limited in their host range (Hoogstraal and Aeschlimann, 1982). Temporary parasite species can mostly not afford high levels of host specificity and must maintain the ability to infest a broader range of different hosts (Fain, 1994; Hoogstraal and Aeschlimann, 1982; Walker et al., 2003). Also in the present work,

30 examined ticks of the temporary hard tick species Haemaphysalis microcebi were observed to infest all four host species. Likewise, the temporary and periodic Trombiculidae mite Schoutedenichia microcebi exhibited low host specificity, as it was found to infest all investigated host species (chapter II). Levels of host specificity in heteroxenous helminths can be very different for intermediate and definitive hosts (Chubb et al., 2009). In the course of parasite evolution, additional hosts can be added to the life cycle by two different mechanisms. The addition of a new intermediate host, which is at a lower trophic level than definitive host is called “downward incorporation”. The addition of a host species to the parasite life cycle, which is a predator of the original host species is called “upward incorporation”. Parasite reproduction is then typically suppressed in the original host as it becomes an intermediate host (Parker et al., 2003). Based on the length of period in co-evolution, either the specificity to the definitive host (downward incorporation) or to the intermediate host (upward incorporation) is more pronounced. However, overall high and overall low host specificity are also common cases (Baker, 2008; Deplazes et al., 2012; Hiepe et al., 2006; Parker et al., 2003). Although, mouse lemurs, E. myoxinus, and R. rattus harbored different species within the morphotype Subuluroidea fam. gen. spp. in the present study (chapter III), the ability of the parasites to infect a definitive host of another species cannot be excluded. As specific arthropods might be eaten only by specific predators, infections could also be restricted by the selective uptake of intermediate hosts with the diet, mediated by the ecological niche of the definitive host. Since intermediate host identity for the two heteroxenous gastrointestinal morphotypes in this study (Subuluroidea fam. gen. spp. and spirurid egg 1) and the detailed composition of the definitive host´s diet remain unclear, conclusions on host specificity are difficult to draw and would require additional host-parasite-network analyses to disentangle these relationships.

3.2 Host related factors affecting parasite prevalences

3.2.1 Host population density Although host population density is commonly known to be associated to an increasing pathogen infection risk (Arneberg, 2002), this relationship was not exhibited by most parasite types studied in this work. Only two types of ectoparasites (ticks and sucking lice) occurred in higher prevalences in response to higher host population densities (chapter II). Pathways leading to higher parasite prevalences in dense populations are mediated differently for homoxenous parasites, which are mainly transmitted by direct contact (e.g. sucking lice, 31

Laelaptidae and Atopomelidae mites, oxyurid nematodes), homoxenous parasites which are mainly transmitted via the environment (e.g. Trombiculidae mites, Strongyloides nematodes) and heteroxenous parasites, which need at least two hosts to complete their life cycles (e.g. most ticks, Subuluroidea fam. gen. spp., spirurid nematodes). Infections with homoxenous parasites mainly transmitted directly between individuals depend on close body contact between hosts, which could increase in dense populations due to the higher probability of social interactions between individuals. The results on sucking lice prevalences were congruent with this hypothesis. However, other homoxenous parasites with similar transmission pattern like ectoparasitic Atopomelidae and gastrointestinal pinworms (Enterobiinae gen. sp. and Lemuricola sp.) did not show a similar response to variations in host population density. Since the transmission pathways of the Atopomelidae should be similar to those of sucking lice, the lacking effect of host population density remains unclear in this case. However, the social organization of the studied hosts might explain the lacking density effect for pinworms and laelaptid mites. Since mouse lemurs, the hosts of the pinworms, forage alone and mating is restricted to a very short period of the year, most cases of pinworm transmission will happen between individuals of the same social sleeping group (Lucatelli et al., 2020). Laelaptid mite infections are probably mediated via group-specific sleeping sites, as the nidicolous mites live and reproduce in the debris of their host´s nest (Maaz, 2018). At least for mouse lemurs, the size and composition of these sleeping groups is rather constant and independent from population density (Radespiel, 2000; Weidt et al., 2004). The infection risk for homoxenous parasites with environmental transmission is depending on the concentration of infective parasite stages in the environment, e.g. soil. Higher strongyle nematode prevalences in dense populations of black rhinoceroses (Diceros bicornis), for example, were related to the increasing number of hosts excreting parasite eggs and hence drive parasite abundance (Stringer and Linklater, 2015). Such a relationship between host population density and prevalences of ectoparasitic Trombiculidae mites and endoparasitic Strongyloides spp. nematodes, which are both homoxenous and undergo environmental phases in their life cycle or even experience full environmental generations (only Strongyloides spp.), however, was not observed in our study. Since Trombiculidae mites are not host specific and are also known to feed on numerous other vertebrates beyond mammals, like birds and reptiles (Kampen, 2002; Morand and Krasnov, 2007), Trombiculidae abundance might be rather independent from the population density of the studied host species alone. In contrast, the lack of host population density impact on Strongyloides spp.

32 prevalence may rather be due to the development of an effective immunity by the hosts. A strong developing immunity, which is preventing subsequent infections, is for instance known in mice after initial infections with very low doses of infective S. ratti larvae (Dawkins and Grove, 1982). In ticks, a positive relationship of tick abundance and the population density of a single host species was, for instance, observed in the deer tick (Ixodes dammini) in relation of white- tailed deer (Odocoileus virginianus) abundance in North Amerika (Wilson et al., 1985). Correspondingly, tick prevalence was also positively associated to host population density in this project (chapter II). Since most ticks are not very host specific and all developmental stages have been demonstrated to feed on mouse lemurs (Klein et al., 2018), the increase of feeding success due to the high density of available hosts in dense populations might substantially promote tick abundance and consequently also prevalence. For heteroxenous gastrointestinal parasites (Subuluroidea fam. gen. spp., spirurid nematodes), which require arthropods as intermediate hosts, no association with definitive host abundance was found. However, as information on identity and density of their intermediate hosts are still lacking, no further statement can be made on this case.

3.2.2 Host sex When comparing parasite infections between the sexes, higher prevalences and infection intensities tend to be found in males compared to females (Poulin, 1996; Zuk and Mckean, 1996). For example, exclusive removal of gastrointestinal parasites in male yellow-necked mice from the Italian Alps led to a decreasing parasite load also in female individuals. Since this effect could not be reproduced by removing the parasites in female individuals only, Ferrari et al. (2004) concluded that males are the main drivers of parasite infections in this populations. A similar pattern was also demonstrated for sucking lice in brown mouse lemurs (Zohdy et al., 2012). Also in the present work, sucking lice and Lemuricola sp. pinworms were found in higher prevalences in males than in female hosts. Such differences are often explained by indirect effects of testosterone, which depresses immune function and occurs in higher levels in males than in females (Klein, 2004; Schalk and Forbes, 1997; Zuk and Mckean, 1996). Recent studies, however, demonstrated that the effects of testosterone are more complex. Even protective effects of the hormone against parasite infections could be shown (Ezenwa et al., 2012), and the effects seem to differ between parasite types (Fuxjager et al., 2011). Such complex interactions could also partly explain the lack of clear findings in most of our parasite taxa. Besides possible hormonal effects, sex-specific behaviors are 33 hypothesized as being responsible for most cases of differences in parasite load between males and females (Kraus et al., 2008). Males more likely engage in risky behavior, have larger home ranges, and more social encounters with unknown individuals, which may lead to parasite uptake and transmission (Poirotte and Kappeler, 2019; Soliman et al., 2001; Zuk and Mckean, 1996). Since only prevalences of mainly interindividually transmitted homoxenous parasite types (sucking lice, Lemuricola sp.) were affected by host sex, it is indeed very likely that male behavior was responsible for the results of the present work. If mainly hormonal and immunological mechanisms were relevant, also heteroxenous and environmentally transmitted parasites (e.g. ticks, Subuluroidea fam. gen. spp., Strongyloides spp.) should have had higher prevalences in males, which was, however, not observed. Since this study provides only indirect evidence, further research efforts beyond this work are needed to demonstrate these relationships in detail for the four host species studied here.

3.2.3 Host body condition In many studies in the field of wildlife parasitology, a good body condition is related to elevated levels of parasite infections (Arneberg, 2002; Sánchez et al., 2018). Also this work found mostly positive associations between parasite prevalence and body mass (chapter II, ectoparasites) or body condition (chapter III, gastrointestinal parasites): Laelaptidae and Atopomelidae mites and the gastrointestinal parasite types Lemuricola sp. and spirurid egg 1 showed higher prevalences in hosts with higher body mass or better body condition. Also the GPSR was shown to be positively associated. Sucking lice, however, are the only parasites where higher prevalences were found in hosts with low body mass (chapter II). According to the “well-fed host hypothesis”, hosts with a good body condition are preferred by parasites due to their higher profitability. The hypothesis was confirmed by lab experiments of Christe et al. (2003), showing a clear preference of the ectoparasitic bat mite Spinturnix myoti for hosts with a better body condition. Rafalinirina et al. (2007) also related elevated levels of ectoparasite infestations in brown mouse lemurs (M. rufus) with better body condition to this hypothesis. However, since most gastrointestinal parasites do not actively invade their hosts, but mostly depend on accidental infection, this hypothesis could only explain the ectoparasite results of this study. A positive relationship between host body-condition and prevalences of gastrointestinal parasites is better explained by host age. In the absence of a protective immunity, older individuals, with higher fat reserves and therefore in better body condition (Rakotoniaina et al., 2016) than younger individuals, might have accumulated parasites over time (Bellay et al., 2020). Also the higher feeding capacity of hosts with better body

34 condition, which increases the probability of accidental pathogen ingestion, might lead to higher parasite prevalences and species richness. When relating low body condition and parasite infections, the directionality of interaction often remains unclear. As parasites may cause damage to the bodies of their hosts and withdraw nutrients, blood and body fluids, parasite infections can deteriorate their host´s body condition (Deplazes et al., 2012; Holmes, 1985). On the other side, hosts in bad body condition might not be able to generate an effective immune response to defend against the parasite (Hiepe et al., 2006). As immunity develops over time, the response might also be ineffective in juvenile hosts, which tend to have a low body condition, compared to older individuals, which tend to build up fat reserves (Ladeia-Andrade et al., 2009). Since this age- dependent resistance has often been reported in particular for infections with sucking lice (Nelson et al., 1983), a lacking protective immunity in juvenile hosts is suggested to be responsible for the negative correlation between sucking louse prevalence and body mass found in this study. A similar study, investigating sucking louse infections in gray and golden brown mouse lemurs, however, could not find associations between parasite prevalence and host body condition or age (Klein et al., 2018).

3.2.4 Host diet and social structure Studies on helminth infections in birds, fish and mammals with differing dietary requirements have found a higher parasite diversity in omnivorous compared to herbivorous hosts (Aho et al., 1991; Bell and Burt, 1991; Galaktionov, 1996; Guegan and Kennedy, 1993; Rasmussen and Randhawa, 2018; Springer and Kappeler, 2016). The finding was predominantly explained by omnivorous species feeding on invertebrates, which might serve as intermediate hosts for heteroxenous parasites (Aho et al., 1991; Springer and Kappeler, 2016). Also in the present study, the investigated host species differ in their diet. A large part of the omnivorous mouse lemur diet consists of insects (Thorén et al., 2016) and also the opportunistic black rats are known to feed on arthropods in varying quantities depending the general availability of resources (Clark, 1982). E. myoxinus in contrast, feeds on a frugivorous diet and arthropods are only accidentally ingested alongside with its vegetarian food (Shi et al., 2013). According to this, GPSR was found to be higher in the two mouse lemur species (mean GPSR: 0.899 in M. murinus and 1.261 in M. ravelobensis) and R. rattus (mean GPSR = 1.093) than in E. myoxinus (mean GPSR = 0.196). In addition, mouse lemurs and black rats harbored from eight (M. murinus) to eleven different gastrointestinal parasite morphotypes (M. ravelobensis, R. rattus), while the western tuft-tailed rat was only infected by three morphotypes 35

(Subuluroidea fam. gen. spp., Subuluroidea-like-egg, spirurid egg 1). Finally, prevalences of the heteroxenous Subuluroidea fam. gen. spp. were significantly higher in the omnivorous mouse lemurs than in the frugivorous E. myoxinus. Taken together, these findings on the four studied small mammal hosts strongly support the hypothesis that the dietary regime of host species impacts their gastrointestinal parasite load. In addition to its differing dietary requirements, the western tuft-tailed rat can also be clearly distinguished from the other studied host species by its solitary lifestyle during activity but also during the resting period (Shi et al., 2013). Social encounters enable animals to transmit stationary ectoparasites and eggs of homoxenous gastrointestinal parasites to their social partner. Although the effects of sociality on parasite infections are still debated (Altizer et al., 2003; Rifkin et al., 2012), Lucatelli et al. (2020) could show in a meta-analysis of 75 studies on parasite infections in bird and mammal communities that social structure is directly linked to parasite load. Also Bordes et al. (2007) found a positive relationship between the diversity of mainly interindividually transmitted ectoparasites and the level of sociality in rodents. As a consequence, the solitary lifestyle of E. myoxinus can be assumed to provide less opportunity for the transmission of parasites between individuals (Rifkin et al., 2012). In contrast, higher rates of social encounters in populations of the gregarious mouse lemurs, forming sleeping groups (Radespiel, 2000; Weidt et al., 2004), and black rats, living in large social communities (Münster, 2003), should promote the transmission of interindividually transmitted homoxenous parasites (Strona and Fattorini, 2014). Such an effect might explain the higher prevalences of Laelaptidae mites in black rats and mouse lemurs compared to E. myoxinus (chapter II), since these nest-associated parasites are shared between individuals at the sleeping sites. Finally, since prevalences of both heteroxenous parasites, which might be rather affected by dietary differences, and homoxenous parasites, which are more influenced by social structure, are affected, the differences in parasite diversity between E. myoxinus and the other host species can most likely be explained by the interaction of both factors.

3.2.5 Host sleeping site ecology Some results of the present work indicate differences in parasite infection patterns that may be related to the sleeping site ecology of the different host species. Infections of some investigated mainly interindividually transmitted and homoxenous morphotypes are depending on host individuals meeting at their sleeping sites: populations of the nidicolous Laelaptidae mites are living in the debris of the sleeping sites of their hosts (Maaz, 2018) and

36 also pinworm (Enterobiinae gen. sp., Lemuricola sp.) transmission is restricted to the nests, since eggs are mostly not excreted with the feces, but deposited around the anus of the host (Hugot et al., 1999). Eventually, they are dispersed by auto- or allogrooming or accidentally picked up by a new host at the sleeping site. The more sheltered and the more frequently visited these sleeping sites are, the better are the conditions for transmission of the mentioned parasite types. The absence of homoxenous gastrointestinal parasites in the solitary E. myoxinus (chapter III) has already been stated in the previous subchapter. In comparison, the more gregarious mouse lemurs and black rats provide better conditions for the transmission of such homoxenous parasites. However, they differ in the use and quality of their sleeping sites. While gray mouse lemurs and black rats are using well protected spots in wooden tree holes or in dens in the ground (only R. rattus) over longer periods of time (Münster, 2003; Radespiel et al., 2003; Ramiarinjanahary et al., 2001), golden-brown mouse lemurs are more flexible in their choice of sleeping sites and use them for shorter periods of time. Besides in wooden tree holes, M. ravelobensis often sleeps in ephemeral, self-built leaf nests and has also been observed sleeping under a pile of leaves on the ground (Radespiel et al., 2003; Thorén et al., 2010). These differences in sleeping site quality and usage duration give rise to the prediction that M. ravelobensis should have lower prevalences of pinworms and nest- associated Laelaptidae mites. In congruence with this expectation, Laelaptidae mites and Lemuricola sp. pinworms were indeed found in significantly lower prevalences in M. ravelobensis than in M. murinus and R. rattus. For other parasite types, however, the sleeping habits of M. ravelobensis may rather offer advantages. For example, chigger mites (Trombiculidae) are periodic parasites: the main part of the chigger population lives as arthropod predators in the soil and leaf litter, and only the larvae feed as ectoparasites on body fluids of vertebrate hosts (Maaz, 2018). These are typically infested by contact with leaf litter or soil (Kampen, 2002). Also, Strongyloides spp. are soil-borne parasitic nematodes that can establish populations in the environment, since they can optionally insert a soil-dwelling environmental generation between parasitic generations (heterogonic cycle) in addition to successive parasitic generations (homogonic cycle) (Viney and Lok, 2015). Besides possible autoinfections (Olsen et al., 2009) and lactogenic infections from mother to offspring (Viney and Lok, 2015), most hosts are infected by soil-dwelling Strongyloides larvae penetrating the skin, when coming into contact with the ground (Baker, 2008; Olsen et al., 2009; Smith, 1999). The higher prevalences of Trombiculidae mites and Strongyloides spp. in golden- brown mouse lemurs, compared to M. murinus and R. rattus, may be attributed to their 37 sleeping habits, which involve more frequent contact with leaf litter and soil compared to the other two species.

3.2.6 Invasive versus endemic hosts The co-invasion of parasites along with their invasive hosts is an important aspect when studying ecological impacts of invasive species (Lymbery et al., 2014). Consequences for native taxa can be substantial, if they are susceptible to the invasive parasite and the pathogen is even more virulent in the invaded communities than in the invasive species (Morand et al., 2015). The most prominent example is probably the introduction of Plasmodium relicta, the causative agent of bird malaria, by invasive bird species (and the vector mosquito Culex quinquefasciatus) to endemic bird populations of Hawaii (Lymbery et al., 2014; Warner, 1968). Multiple extinction events and the ongoing threats to the Hawaiian honeycreepers (Carduelinae) can be attributed to this pathogen (Pang-Ching et al., 2018; Sehgal, 2015). Also rats of the genus Rattus were reported to have introduced their co-invasive parasites to endemic wildlife: for example, the blood parasite Trypanosoma lewisi was introduced to primates in Brazil (Maia da Silva et al., 2010) and the nematode Trichuris muris to endemic rodents in North Amerika (Smith and Carpenter, 2006). Pathogen spillover from R. rattus to Malagasy wildlife was, however, not reported until now (Morand et al., 2015). Although no clear pathogen spillover could be demonstrated in this work either, there are two observations that deserve to be mentioned in this context. Black rat specific Hoplopleura sp. sucking lice could be found on two individuals of the native E. myoxinus. However, since only single lice were found, an accidental rather than a successful permanent infestation with associated parasite reproduction was assumed. Nevertheless, the finding indicates close spatial association between endemic and invasive rodents, since sucking lice do not survive longer than a few hours without their host (Light et al., 2010). The second observation concerns the simultaneous presence of the gastrointestinal parasite morphotype spirurid egg 1 in all investigated host species (chapter III). In R. rattus, the presence of the spirurid nematode Protospirura muricola was assumed based on molecular results. This spirurid species, primarily harbored by rodents in the tropics (Smales et al., 2009), was previously reported to infect primates and other wildlife (Kouassi et al., 2015; Petrzelkova et al., 2006; Smales et al., 2009). Since the presence of P. muricola outside of continental Africa was always associated to the cosmopolitan rodents R. rattus and R. norvegicus as reservoir hosts, a pathogen spillover from R. rattus to the endemic mouse lemurs and tuft-tailed rats could be responsible for the excretion of spirurid egg 1 in these hosts. The higher prevalences in R. rattus (49.7%)

38 than in the endemic species (8.0-9.8%) might further support this hypothesis. However, it could not be verified, since a molecular identification of the eggs excreted by the endemic hosts was not possible. According to the “enemy/parasite-release hypothesis”, the success of invasive species can be partly attributed to the absence of natural predators, pathogens and parasites (Colautti et al., 2004). In terms of parasites, this could be shown for introduced black rat populations on Mediterranean islands, which exhibited a reduced gastrointestinal helminth diversity (Gouy de Bellocq et al., 2002). In addition, a study comparing parasite species richness between populations of R. rattus worldwide have found lowest parasite diversity in Malagasy black rat populations (Wells et al., 2015). Also in the present work, both EPSR and GPSR were lower in the invasive black rats compared to the native mouse lemurs. In addition, black rats were not infested by fur mites (Atopomelidae), although such infestations of Rattus spp. are known in other parts of the world (Bochkov and Fain, 2003). It is possible that these host-specific parasites were not co-introduced during colonization of Madagascar and are hence absent today from Malagasy black rat populations. Although R. rattus showed no difference in EPSR compared to E. myoxinus and even had a higher average GPSR, the comparison of R. rattus to the endemic E. myoxinus is difficult, since the species differ greatly in both social structure and diet.

3.3 Habitat-related factors affecting parasite prevalences

3.3.1 Effects of vegetation structure Vegetation is generally known to substantially influence microclimate of a habitat by providing shade, access, evaporation, storage of water, and the formation of organic soil (Vanwalleghem and Meentemeyer, 2009). In a study on the effects of forest clearing on the microclimate of tropical lowland forests in Costa Rica, temperature in cleared areas was found to be significantly higher and atmospheric humidity significantly lower than in the surrounding pristine forests. Since differences peaked during the day, they were related to the increased solar radiation in cleared areas (Fetcher et al., 1985). For their development and reproduction, parasites depend on certain microclimatic conditions. Although many parasite species have developed adaptations to survive suboptimal conditions (Andersen and Levine, 1968; Perry, 1999), arthropod ectoparasites like ticks (Heath, 1981) and fleas (Heeb et al., 2000) but also free-living stages of parasitic nematodes (Brown and Gaugler, 1997) were shown to depend on suitable levels of humidity to avoid desiccation. 39

In the third chapter, the effects of two vegetation condition parameters (vegetation clearance and forest maturation) on prevalences of gastrointestinal parasites were investigated. As expected, hosts captured in more open forests, interspersed with savannah-like grassy vegetation, showed lower prevalences of both heteroxenous parasites (Subuluroidea fam. gen. spp. and spirurid egg 1) and the homoxenous Strongyloides species. Since free-living heterogonic populations and developing homogonic larvae of Strongyloides spp. depend on a moist humus layer (Faust and Giraldo, 1960), areas with cleared vegetation and dry soils without humus are unsuitable habitats for this gastrointestinal parasite morphotype. The heteroxenous morphotypes Subuluroidea fam. gen. spp. and spirurid egg 1 require arthropod intermediate hosts to complete their life cycle. Arthropod abundance and diversity was previously shown to be lower in more open and secondary vegetation (Cole et al., 2016; Gardner et al., 1995) which was explained by unfavorable microclimatic changes and a lack of organic resources in these places. Unfavorable conditions for the arthropod intermediate hosts may therefore also explain the low prevalences of Subuluroidea fam. gen. spp. and spirurid egg 1 in this study. Conversely, prevalences of the homoxenous pinworms (Enterobiinae gen. sp. and Lemuricola sp.) did not differ along a gradient of vegetation clearance. The absence of such an impact on the two pinworm species is most likely related to their simple life cycle with its direct mode of transmission. Since the eggs are transmitted in close body contact or at the sleeping sites, they may not be much affected by the outer environmental conditions but rather by the stable microclimate of the host´s body or in the protected nest environment. However, pinworm prevalences were influenced by another studied vegetation factor. Alongside with increasing forest maturation, a gradient from low, but dense secondary forest to mature primary forest with taller old growing trees, prevalences were decreasing for Enterobiinae gen. sp., but increasing for Lemuricola species. As already discussed, pinworm infections should be mostly associated to the host´s sleeping sites, since these spots typically show high contamination rates with pinworm eggs and provide opportunity for interindividual contact. Prevalence differences may hence be related to the availability of tree holes, which in turn should be linked to the density of old and large trees. Such sleeping sites should be available in greater numbers in an old-growth primary forest (Carlson et al., 1998), so that infection risk and prevalences would increase in such microhabitats. While this argument may explain the increasing prevalence of Lemuricola sp. under higher forest maturation, it cannot explain the findings in Enterobiinae gen. species. Future studies will be needed to explore the

40 link between sleeping site ecology (type and host-specific usage patterns of sleeping sites), microhabitat characteristics and homoxenous parasite load in more depth.

3.3.2 Edge effects Habitat edges, in particular when the two bordering habitat types are largely different, generate strong ecological contrasts that can affect the vegetation and biota on both sides of the edge up to a considerable depth (Murcia, 1995). In the present study, two different types of habitat, savannah and dry deciduous forest, bordered each other at the forest edges. The savannah either consisted of grassy vegetation on sandy soils where shrubs and bushes were rare (ANK) or of savannah interspersed with palm trees (Bismarckia nobilis) in varying densities (MAR). Two studies on edge effects of vegetation in northwestern Malagasy dry forests showed that vegetation differed significantly between forest edge and interior as tree stem densities were lower (Malcolm et al., 2016) and understory vegetation less high and dense at the edge (Andriatsitohaina et al., 2020a). The exposure to the open savannah and edge vegetation with reduced density typically goes along with a reduced protection against abiotic factors like sun and wind. Investigations on microclimate gradients across rainforest edges in New Zealand, for example, showed major differences of abiotic parameters between edge and interior: wind speed and air temperature increased and humidity decreased up to a distance of 40 m to the edge (Davies-Colley et al., 2000). In addition, also a lower proportion of organic matter in the soil at the edge was confirmed up to a distance of 80 m from the forest edge in Brazilian forests (Camargo and V. Kapos, 1995). In analogy to the effects of vegetation clearance (see above), edge-related abiotic changes can be expected to generate unfavorable conditions for the development, reproduction and transmission of parasites. Species that spend longer periods in the outer environment will be particularly affected. In this study, such edge-related effects, represented by the two parameters “distance to edge” and “edge percentage”, where shown to decrease prevalences of almost all investigated parasite types (chapter II, III). In addition, EPSR and GPSR were lower in hosts living at the edge than in hosts from the forest interior. In the study of Andriatsitohaina et al. (2020b) investigating vegetation edge effects in the same area, most vegetation characteristics like the number of seedlings and lianas and the diameter of larger trees were affected by edge proximity up to a distance of 50 m from the edge. The density of smaller trees (up to 360 m) and the height of larger trees (up to 460 m), however, were impacted up to greater distances, which is remarkable, since most edge effects do not penetrate deeper than 150 m into the forest (Laurance, 2000). However, also edge effects on 41 parasite prevalences in the present work extended to more than 350 m from the edge. The depth of edge influence on ectoparasite prevalences (ticks, Trombiculidae and sucking lice in chapter II) even exceeded 750 m. The analogous findings on parasite prevalences in this study and vegetation in the same area by Andriatsitohaina et al. (2020b) provide further evidence for the relationship between vegetation and parasite prevalence in the context of edge effects. The microclimatic mechanisms that lead to impaired development, reproduction, and transmission in altered vegetation have already been discussed for gastrointestinal parasites in the previous subchapter. Just like Strongyloides spp., the soil-dwelling Trombiculidae mites depend on a moist environment with a high proportion of organic material (Kampen, 2002; Maaz, 2018). Although ticks do mostly not live directly in the soil, they also strongly depend on certain levels of humidity (Kakuda et al., 1990). Especially during the molting phase, a dry environment leads to significantly higher tick mortality (Walker et al., 2003). Since sucking lice as stationary parasites and Laelaptidae mites as nest-associated parasites should be more protected from environmental influences, negative impacts of edge proximity on their prevalences were rather unexpected. One study, however, detected higher prevalences and diversity of sucking lice in moist compared to dry habitats of small African mammals (Oguge et al., 2009). Moreover, mites of the Laelaptidae family were found to be susceptible to desiccation if humidity in the host´s nest is too low (Wharton and Kanungo, 1962). The microclimate on the host's body and within the sheltered sleeping sites, however, should buffer the abiotic environmental conditions to some extent. In congruence with this expectation, the slope of the curve with sucking louse prevalence as a function of distance to the edge was flatter than for the other ectoparasite types, and significant negative edge effects in Laelaptidae mites were detected only in the forest fragments but not in the complete data set. No negative edge effects were found for Atopomelidae mites, both pinworm species and the morphotype spirurid egg 1. The lack of negative edge effects on prevalences of Atopomelidae mites and the two pinworm species (Enterobiinae gen. sp., Lemuricola sp.) might again be explained by the buffering microclimate on the host's body and in the sheltered sleeping sites. The lack of negative edge effects on spirurid egg 1, however, is contrasting to the results for the other heteroxenous morphotype Subuluroidea fam. gen. spp., which was negatively affected by proximity to the edge. This, however, may be related to the high prevalences of spirurid egg 1 in R. rattus, which are known to thrive in degraded habitats and access most natural landscapes coming from the edge (Andriatsitohaina et al., 2020b; Delgado et al., 2001; Goodman, 1995; Ruffell et al., 2014). Since the species identity, intermediate hosts and

42 environmental resistance of the spirurid nematode species in the black rats are, however, not conclusively elucidated, additional research efforts are needed to further explain this issue.

3.3.3 Effects of fragmentation and habitat size The most basic parameter in our set of tested prediction variables for the detection of HF impacts on parasite infections is the comparison of prevalences between hosts from patches of continuous forest and forest fragments. Prevalences of ticks, Trombiculidae mites, Strongyloides spp. nematodes and the EPSR were higher in hosts from the continuous forest. Similarly, the size of forest patches was positively associated with prevalences of these parasite types and EPSR. In general, habitat size is used to explain species richness of free- living organisms within the framework of species-area relationships (SAR), since larger habitat patches support broader niche dimensions by providing more resources (Simberloff, 1972; Wilson and MacArthur, 1967). However, since parasite diversity is mediated by the nested structure of factors like host specificity and the density and distribution of suitable hosts, the classical mechanisms underlying the SAR are limited in their application to parasites (Strona and Fattorini, 2014). In addition, also resource constraints for the parasites could not be identified. It is more likely that vegetation and microclimatic conditions caused additive edge effects in fragments of rather limited size (Figure 4.1).

Figure 4.1: Schematic illustration of edge effects from opposite sides of a large (a) and a small (b) circular forest fragment. When overlapping, effects become additive and hence stronger in smaller compared to larger fragments. Modified after Malcolm et al. (2016).

Those amplified edge effects in smaller fragments of dry forest in northwestern Madagascar were already demonstrated by Malcolm et al. (2016). Additive effects of edges emerge, if edges affect the ecological conditions within a forest fragment from different directions simultaneously and thereby add up in complex ways. Such additive edge effects might in fact 43 explain the detected fragmentation effects, since those parasites (ticks and Trombiculidae mites, as temporary ectoparasites, and Strongyloides spp. with its heterogonic free-living generations) can be assumed to be particularly vulnerable to environmental changes.

3.4 Implications for conservation The results of the present study have clearly shown that habitat degradation associated with HF negatively affects the diversity of ectoparasites and endoparasites of small mammals in dry deciduous forests of northwestern Madagascar. As such, this study has clear conservation implications for a taxonomic group of high ecological relevance. Parasites in threat, however, are not only a local phenomenon. In fact, parasite diversity is threatened worldwide (Dunn et al., 2009). Due to climate change alone, 5-10% of the world’s parasite species are predicted to become extinct by the year 2070. In this context, ectoparasites are considered as particularly vulnerable (Carlson et al., 2017a). The second factor driving parasite extinctions are coextinctions of host-specific parasite species alongside with their hosts (Dunn et al., 2009; Durden and Keirans, 1996). However, host extinction is not even needed to drive host- specific parasite species into extinction, as chains of infection break quickly when hosts are rare and separated into small subpopulations (Bush and Kennedy, 1994). As a result of this development, Carlson et al. (2017) estimated that for instance up to 30% of parasitic helminth species will go extinct until the year 2070. In addition, parasites have also been eradicated by human intervention in order to protect their hosts. The most prominent example is a not even described sucking louse species of the black-footed ferret (Mustela nigripes), which became extinct during a breeding program to conserve the host (Gompper and Williams, 1998). Many more cases certainly exist that were not even registered due to the lack of knowledge on parasite diversity (Rózsa and Vas, 2015). In contrast to this upcoming but rather neglected mass extinction of parasite species, parasites are widely expected to become increasingly influential by infecting endemic wildlife under progressing climate change and anthropogenic habitat modification (Barrett et al., 2013; Lymbery et al., 2014; Thompson et al., 2010). However, this expectation refers to a rather low number of invasive pathogens with high host flexibility like Giardia spp., Cryptosporidium spp. and Blastocystis spp., which exhibit a simple homoxenous life cycle and low host specificity (Wells and Clark, 2019). However, zoonotic, heteroxenous parasites with humans or domestic animals as definitive hosts and low intermediate host specificity (e.g. Echinococcus spp. and Toxoplasma gondii) or parasites of humans and domestic animals transmitted by vectors (e.g. Leishmania spp. and Trypanosoma spp.) are also increasingly found in wild animal populations (Monis and Thompson, 2003;

Spencer and Irwin, 2020; Tenter et al., 2000; Thompson et al., 2010; Vaz et al., 2007; Waindok et al., 2021). Those pathogens will become particularly threatening to wildlife, when species are already endangered and populations are small (Holmes, 1996; Smith et al., 2009). However, the vast majority of parasite species are endemic and have a pronounced specificity for host and habitat (Carlson et al., 2020). They are adapted to certain ecosystems and cause impacts that have far more positive than negative consequences (Dobson et al., 2008; Gómez and Nichols, 2013; Lafferty et al., 2008; Marcogliese, 2005, 2004; Mouritsen and Poulin, 2005; Thomas et al., 1999). The parasites that were particularly affected by habitat changes in this study are very likely endemic habitat specialists that co-evolved with the studied host species. Native parasite taxa contribute significantly to biomass, energy flow and the stability of ecosystems and promote biodiversity (Lafferty et al., 2008; Mouritsen and Poulin, 2005). A good example is provided by the study of Schall (1992), who demonstrated that the coexistence of two Caribbean Anolis lizard species was driven by the Anolis-specific vector- borne parasite Plasmodium azurophilum. The higher susceptibility of the more dominant species to the parasite ensured a regulation of its population and thus prevented the displacement of the weaker lizard species. Considering these important functions of parasites and the fact that they account for nearly half of total biodiversity, consequences of losing a significant portion of this diversity are likely to be severe. As a result, reasonable conservation efforts should take the entire ecosystem into account in which endemic parasites must not be forgotten. Invasive pathogens, however, should be kept under strict surveillance due to their threat to endangered species and a potential spillback to humans.

3.5 Conclusions The present work investigated how ecto- and gastrointestinal parasite infections of four small mammal species from fragmented dry forests in northwestern Madagascar respond to a changing environment. Parasite life cycle traits such as long environmental periods, free living generations or the dependence on arthropod intermediate hosts were identified to increase parasite susceptibility to microclimatic changes caused by altered vegetation conditions at the forest edge and in small forest fragments. The expected impacts of HF and habitat degradation that may increase host susceptibility to parasite infections were not observed. However, these effects may have been present but masked by negative impacts on parasite biology. Considering the fact that most edge effects are penetrating less than 150 m into the forest interior (Laurance, 2000), it is noteworthy that the edge effects influencing 45 parasite prevalences were penetrating up to 750 m into the forest. Although an invasive host species (R. rattus) was also studied, no transmission of invasive parasite species to native hosts was documented with certainty. Nevertheless, there is evidence of close contact between host species, which may allow the transmission of pathogens in the future. Climate change and host extinction are regarded as the main drivers of an imminent biodiversity crisis of parasitic species which is expected to aggravate in the near future (Carlson et al., 2017). By providing first evidence that habitat changes can also have a direct impact on parasite diversity, this study added a whole new dimension to this debate. However, questions regarding habitat connectivity, as an important cofactor of HF, could not be answered within the scope of this study and questions concerning transmission and detailed life history of the particularly heteroxenous gastrointestinal parasites remain unclear. Future studies that include detailed host-parasite network analyses are needed to elucidate these aspects by investigating parasite dispersal, transmission and identity of intermediate hosts.

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List of Abbreviations acc. no. accession number ANK Ankarafantsika National Park asl above sea level bp base pairs cf. confer cox1 cytochrome c oxidase unit 1 DNA deoxyribonucleic acid e.g. for example (lat.: exempli gratia) EPSR ectoparasite species richness fam. family g gram gen. genus GPS Global Positioning System GPSR gastrointestinal parasite species richness HF habitat fragmentation ITS internal transcribed spacer MAR Mariarano Classified Forest SAR species area relationship sp. species spp. species (Pl.)

Acknowledgements First and foremost, I would like to thank my two main supervisors, who gave me the opportunity of conducting my PhD thesis as a joint venture of their two institutes and guided me safely through many scientific obstacles over the past four years. From a parasitological point of view, this was Prof. Dr. Christina Strube, PhD, who continuously provided helpful advice and new ideas and was always able to motivate me to give my best. From the ecological perspective, this was Prof. Dr. Ute Radespiel, who deeply impressed and inspired me with her inexhaustible energy. Conversations with her, always at eye level, have greatly influenced me in the development of critical thinking and self-organization and always remembered me to enjoy what I am working on.

I would like to thank the other two members of my supervision group, Prof. Dr. Nicole Kemper and PD Dr. Oliver Schülke, for the positive and constructive feedback, helpful suggestions and straightforward communication.

The time in Madagascar was a very impacting episode of my life. I would like to thank Bertrand Andriatsitohaina and Malcolm S. Ramsay for enjoying, sharing, organizing and mastering these adventures with me.

Samples and data for this work would certainly not have been collected if Prof. Dr. Solofonirina Rasoloharijaona, Dr. Rindrahatsarana Ramanankirahina, Dr. Romule Rakotondravony and Prof. Dr. Shawn Lehman had not supported this enterprise to the best of their abilities. In addition, samples would certainly never have left Madagascar without their energetic help with all the paperwork. Many, many thanks!

Leonie Baldauf, Fernand Fenomanantsoa, Jack O’Connor, Quinn Parker, Olivia Pilmore- Bedford, Herinjatovo Rakotondramanana, Miarisoa Ramilison, Onjaniaina Gilbert Razafindramasy, Simon Rohner and Harry Skinner helped installing transects, caught many mouse lemurs and rats and assisted gathering ticks and turds. Johnny, ZamanDidy, Bernadette, Eva, Felix, Ginot, Jose and Rafidi protected, cooked, guided, lived, learned, laughed and danced with us in the many camps in the field. Nothing would have worked without you, thank you so much.

Additionally, I would like to thank Ursula Küttler, Daniela Jordan, Patrick Waindok, PhD and Annette Klein, PhD for their enormous help, without which I would not have been able to analyze a single sample. With giving me her tent, Annette also provided me with a home and shelter in the forest. Furthermore, thank you to Dr. Andrea Springer and Dr. Ariel Rodriguez, who were always ready to assist if I had any questions or problems.

Thank you to my colleagues at the Institute of Zoology and the Institute for Parasitology. A lot of conversations, encounters and friendships have brightened many days and shaped me intellectually and as a person. I could not have hoped for better colleagues. Thank you for being such great people!

I would also like to thank my parents, who have enabled me to follow my path and always stimulated my interest in nature and everything that lives. My whole family and my friends have never doubted me and have always encouraged and supported me in my progress. I can never thank you often enough for that.

My final thanks go to Hilke. Thank you for being always by my side, supporting me and sharing all the good but also the bad moments. What would I be without you?