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Habitat Partitioning and Ecological Niches of Lizard Species in Karst

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Habitat Partitioning and Ecological Niches of Lizard Species in Karst Population structure and behaviour of the European hedgehog in an urbanized world Inaugural-Dissertation to obtain the academic degree Doctor rerum naturalium (Dr. rer. nat.) submitted to the Department of Biology, Chemistry and Pharmacy of Freie Universität Berlin by Leon Marian Fynn Barthel 28. March 2019 Berlin Erstgutachter/in: First reviewer: Dr. Anne Berger Zweitgutachter/in: Second reviewer: Prof. Dr. Heribert Hofer Tag der Diputation 13.09.2019 To my beloved family, who support me and created my childish interest and love of nature. Dedicated to my father Bernhard Klein-Barthel *8.3.1954 †12.09.2017 This doctoral thesis was part of the ‘Igel in Berlin Project’ of the Leibniz Institute for Zoo and Wildlife research within the Bridging in Biodiversity Science (BIBS) Project of The Berlin Brandenburg Institute of Advanced Biodiversity Research (BBIB). The work was conducted under the supervision of: Dr. Anne Berger Prof. Dr. Heribert Hofer Summary Summary Since humans evolved, they have influenced and changed their environment, which started with hunting pressure and has culminated in climate change. Urbanized areas are arguably the most altered environments on earth, with the process of urbanization transforming natural landscapes in into human-dominated areas. Previous research has found urbanized areas are associated with higher biodiversity, provide refugee habitats for species from various taxa and support high population densities. However, high urbanization can also lead to declining population numbers, local extinction, higher invasion rates of species and potential yet undescribed consequences. Especially the consequences of elevated stressors, which are not exclusive to cities, but are more pronounced than in natural habitats, still need to be elucidated. Therefore model species for the urban living wildlife have to be identified. The Western European hedgehog (Erinaceus europaeus, hereafter hedgehog ) could serve as such a model species as it is geographically widespread. These days, hedgehogs are found in higher density close to urbanised areas while its numbers are declining in some areas of its range. Furthermore, hedgehogs might suffer from the densification of urban areas. The construction of infrastructure causes fragmentation and fragmentation can impede the movement of individuals. This fragmentation can influence gene flow between subpopulations when there is no or only restricted access to mates. Hedgehogs, in particular, could be affected by their restricted dispersal and susceptibility to barriers. Thus, the species characteristics and ecology make them an appropriate model species to understand the effect of humans on small ground-dwelling overlooked species in cities. Therefore the genetic diversity and behavioural plasticity of hedgehogs in a suitable study site like Berlin have to be investigated. In the first genetic study on hedgehogs in a city of this size (~1050 km²), we found, against our expectations, no genetic structure in the population. In a different analysis approach, we could identify ‘family-clan’ structures, which could be an early sign of inbreeding in subpopulations. With our study on the genetic structure of hedgehogs and the identification of new genetic markers, we provide the foundation for future projects to identify the effects of urbanisation on genetic diversity of hedgehogs and evidence-based population management in future. Together with the results of the ecological studies and effects of disturbance and fragmentation on the behaviour of selected hedgehog populations we can draw a better picture of small mammals in cities. For the ecological studies, we developed novel attachment methods in a species-specific manner. We improved methods by considering the welfare of the studied animals, the cost i Summary efficiency and flexibility of the attachment system. This system enabled us to collect spatial and temporal high-resolution data with longer durations than ever before (GPS units). Thus it was possible to follow hedgehogs through an occurring festival in a semi-natural park and in a fragmented zoological garden, identifying population and individual coping strategies, which highlight the behavioural flexibility of hedgehogs. While we were able to show that research is necessary at both the population level and individual level, without continued monitoring of population genetic and individual behaviours using specialized techniques such as ours, we will never be able to fully understand the greater intricacies of such complex ecosystem as we have in urban centres. We now have the technologies and methods to make evidence-based management decisions and harbour species in cities. It is clear, that cities need to give nature space. As long as flora, fauna and funga have enough connections between fragmented “green” areas it might help to sustain healthy populations and could even provide source populations in the process of rural restoration. However, it is also clear that cities are not enough to harbour all wildlife alone in the long-term, especially if the remaining green spaces vanish and cities continue to condense. ii Zusammenfassung Zusammenfassung Seit Beginn der Menschheit nimmt der Mensch Einfluss auf seine Umwelt, was mit dem Jagddruck anfing und sich heute durch sekundäre Einflüsse wie Klimawandel auswirkt. Urbanisierte Gebiete sind wohl die am stärksten veränderten Umgebungen der Erde. Der Prozess der Urbanisierung verwandelt Naturlandschaften auf extreme Weise in vom Menschen dominierte Gebiete. In früheren Studien wurde festgestellt, dass urbanisierte Gebiete mit höherer Biodiversität verbunden sind, Rückzugsräume für Arten aus verschiedenen Taxa bieten und hohe Populationsdichten unterstützen können. Eine starke Verstädterung kann jedoch in anderen Fällen auch zu sinkenden Populationsdichten, zu lokalem Aussterben, höheren Invasionsraten und noch nicht bekannten Folgen führen. Insbesondere die Folgen erhöhter Stressoren, wie zum Beispiel Verschmutzung, Lärm und höheren Temperaturen im Vergleich zu ländlichen Lebensräumen müssen noch geklärt werden. Daher müssen Modellarten für die städtische lebende Tierwelt identifiziert werden, die nicht nur verschiedene Taxa sondern auch verschiedene Charakteristika mit sich bringen. Der Braunbrustigel (Erinaceus europaeus, hiernach auch Igel) mit seiner weiten geographischen Verbreitung könnte eine solche Modellart sein. Igel werden heutzutage in höheren Dichten in der Nähe von urbanisierten Gebieten gefunden und nehmen in Teilen ihres Verbreitungsgebietes ab. Es könnte sein das der Igel unter der voranschreitenden Verdichtung der urbanen räume leidet, denn durch seine charakteristische Morphologie ist er durch Barrieren, die in Städten auftreten, unmittelbar betroffen. Diese Fragmentierung behindert die Bewegung von Individuen. Zusammen mit der Verhaltensbiologie der Igel könnte so die genetische Struktur der Igelpopulation in Städten beeinflusst werden. Mit seiner eingeschränkten Ausbreitung und Anfälligkeit für Barrieren könnte der Igel als Modellart für andere bodenlebende Säugetierarten sein, die sonst übersehen werden. In der ersten genetischen Studie an Igeln in einer Stadt dieser Größe (~1050 km²), fanden wir - entgegen unseren Erwartungen - keine genetische Struktur in der Igel Population. In einem anderen Analyseansatz konnten wir „Familien-Clan’ -Strukturen identifizieren, die ein frühes Zeichen für Inzucht in Subpopulationen sein könnten. Mit unseren Studien zur genetischen Struktur von Igeln und zur Identifizierung neuer genetischer Marker legen wir den Grundstein für zukünftige Projekte. Dadurch können die Auswirkungen der Verstädterung auf die genetische Vielfalt von Igeln besser verstanden werden und, wenn nötig, kann evidenzbasiertes Populationsmanagement initiiert werden. Diese Informationen und die Ergebnisse der iii Zusammenfassung ökologischen Studien, in welchen wir den Einfluss eines Musikfestivals und der Fragmentierung der Stadtstruktur auf das Verhalten von ausgewählten Igelpopulationen untersuchten, können dabei helfen, ein vollständigeres Bild von Igeln in Städten zu liefern. Für die ökologischen Studien haben wir eine neuartige Anbringungsmethode artspezifisch entwickelt. Dabei verbesserten wir das Wohlbefinden der untersuchten Tiere, die Kosteneffizienz und die allgemeine Flexibilität bei Studien im Freiland. Dieses System ermöglichte es uns räumlich und zeitlich hochauflösende Daten zu sammeln und dabei den Tieren länger als zuvor mit GPS Geräten zu folgen. So war es möglich, Igel durch ein stattfindendes Festival und in einem fragmentierten zoologischen Garten zu verfolgen, wobei die Reaktion der Population im Allgemeinen und die individuellen Strategien identifiziert werden konnten, die die Verhaltensplastizität von Igeln unterstreichen. Während wir zeigen konnten, dass Studien sowohl auf Population als auch auf individueller Ebene notwendig sind, ist es ohne durchgehendes Monitoring der genetischen Diversität und des individuellen Verhaltens der Population nicht möglich die Feinheiten eines solch komplexen Ökosystems wirklich verstehen zu können. Wir leben in einem Zeitalter, in welchem wir über Technologien und Methoden verfügen, um Wissen zu sammeln und daraus evidenzbasierte Managemententscheidungen zu treffen. Dadurch wird es uns möglich sein, zu naturfreundlichen Städten beizutragen. Es ist klar, dass Städte der Natur Raum geben müssen. Solange Flora, Fauna und Funga über genügend „grüne“ Verbindungen verfügen, können Städte möglicherweise gesunde Populationen aufrechterhalten
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