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Trollius Europaeus in a Fragmented Landscape Reproductive Success, Genetic Diversity and Trait Differentiation in a Nursery Pollinated Plant

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Trollius Europaeus in a Fragmented Landscape Reproductive Success, Genetic Diversity and Trait Differentiation in a Nursery Pollinated Plant Research Collection Doctoral Thesis Trollius Europaeus in a fragmented landscape reproductive success, genetic diversity and trait differentiation in a nursery pollinated plant Author(s): Klank, Charlotte Publication Date: 2011 Permanent Link: https://doi.org/10.3929/ethz-a-007195830 Rights / License: In Copyright - Non-Commercial Use Permitted This page was generated automatically upon download from the ETH Zurich Research Collection. For more information please consult the Terms of use. ETH Library o Diss. ETH N 20049 TROLLIUS EUROPAEUS IN A FRAGMENTED LANDSCAPE: REPRODUCTIVE SUCCESS, GENETIC DIVERSITY AND TRAIT DIFFERENTIATION IN A NURSERY POLLINATED PLANT A dissertation submitted to ETH ZURICH for the degree of Doctor of Sciences presented by Charlotte Klank Dipl. Biol., University of Goettingen born 03.09.1979 citizen of Germany accepted on the recommendation of Prof. Jaboury Ghazoul Prof. William E. Kunin Prof. Alex Widmer Dr. Andrea R. Pluess 2011 CONTENTS SUMMARY English 1 German 2 CHAPTER 1: Introduction Introduction 3 Trollius europaeus and Chiastocheta 7 References 9 CHAPTER 2: Effects of population size on plant reproduction and pollinator abundance in a specialized pollination system. Summary 14 Introduction 15 Material & Methods 17 Results 23 Discussion 28 References 31 CHAPTER 3: Genetic diversity and plant performance in fragmented populations of globeflowers (Trollius europaeus) within agricultural landscapes Summary 36 Introduction 37 Material & Methods 40 Results 46 Discussion 50 References 53 Appendix 58 CONTENTS CHAPTER 4: Conservation implications based on neutral and quantitative genetic differentiation in Swiss Trollius europaeus populations Summary 62 Introduction 63 Material & Methods 65 Results 68 Discussion 71 References 74 Appendix 77 CHAPTER 5: Conclusion Conclusions 84 References 87 ACKNOWLEDGEMENTS 89 CURRICULUM VITAE 91 SUMMARY Summary Many plant species are currently experiencing negative consequences of habitat fragmentation as a result of reductions in population size and disruptions in pollination services. Plants in specialized pollination systems might be especially vulnerable to changes in plant population size and density resulting from land-use changes. Representing such a system, we chose the globeflower Trollius europaeus L. with its pollinating fly Chiastocheta, which also acts as a seed predator at its larval stage as our study system. We performed an assessment of reproductive success and pollinator abundance, neutral genetic diversity survey and a greenhouse experiment to determine the competitive ability and quantitative genetic variation using 19 globeflower populations located in the Swiss Plateau to investigate the effects of habitat fragmentation on reproductive success, genetic diversity and trait differentiation. Our results show that population size negatively influenced reproductive success, while it plant population densities had an increasing effect. Chiastocheta abundance within T. europaeus flowers was independent of plant population size, though Chiastocheta numbers within flowers were inversely correlated to local T. europaeus flower density. Regarding neutral genetic diversity, the overall genetic differentiation was low (FST = 0.033) with a marginal significant isolation by distance (P = 0.060), and no significant effect for population size, population density or pollinator abundance on neutral genetic diversity was found. Regarding the greenhouse experiment to assess the competitive ability and quantitative genetic variation, no negative effects of habitat fragmentation were found. Overall, Chiastocheta abundance was the main driver of reproductive output of T. europaeus through its dual role as an obligate pollinator and seed predator: at least some Chiastocheta flies were needed to secure pollination, but a continued increase in Chiastocheta flies within a flower incurred seed predation costs that greatly reduced reproductive success. Thus high local flower density contributed positively to per capita reproductive output by diluting Chiastocheta abundance within flowers independently of overall population size. Populations of T. europaeus existing within the highly modified landscape of the Swiss Plateau are currently able to persist and reproduce and show no signs of negative habitat fragmentation effects. Our study highlights the importance to carefully assess what determines the quality of population persistence – in our case rather plant density than pure plant number – and shows that a good understanding of the pollination system and population dynamics is needed to make sound management decision. 1 ZUSAMMENFASSUNG Zusammenfassung Viele Pflanzenarten sind von den Auswirkungen der Habitatfragmentation betroffen, da diese häufig entweder die Populationsgrösse reduzieren oder die Bestäubungsmechanismen gestört werden. Pflanzen mit einem besonders spezialisierten Bestäubungssystem werden im Allgemeinen als besonders anfällig für solche Störungen erachtet. Die Trollblume Trollius europaeus ist durch solch ein System charakterisiert: Die Fliegen der Gattung Chiastocheta sind die alleinigen Bestäuber, gleichzeitig ernähren sich ihre Larven auch von den Samen der Trollblume. In dieser Studie untersuchten wir die Auswirkungen der Landschaftszersiedelung anhand einer Feldstudie zur Bestimmungen der pflanzlichen Reproduktion und der Anzahl der Bestäuber, einer Studie zur Bestimmung der neutralen genetischen Diversität und Gewächshausexperimenten zur Konkurrenzfähigkeit und quantitativen genetischen Differenzierung in 19 T. europaeus Populationen im Schweizer Mitteland. Unsere Ergebnisse zeigen dass die Samenproduktion negativ durch die Populationsgrösse beeinflusst wurde, während die Pflanzendichte einen positiven Effekt hatte. Die Anzahl der Chiastocheta war unabhängig von der Populationsgrösse, allerdings kleinräumig positiv mit der Pflanzendichte korreliert. Die neutrale genetische Differenzierung war niedrig (FST = 0.033), und zeigte auch keine signifikante isolation-by-distance (P = 0.060). Weiter waren Populationsgrösse, Pflanzendichte und Bestäuberanzahl nicht mit der genetischen Diversität korreliert. Die Gewächshausexperimente zur Konkurrenzfähigkeit und quantitativen genetischen Differenzierung zeigten ebenfalls keine signifikanten Effekte, die auf negative Auswirkungen der Habitatfragmentation schliessen lassen. Insgesamt zeigen unsere Ergebnisse dass Chiastocheta der Hauptfaktor für den Fortpflanzungserfolg der Trollblume aufgrund ihrer doppelten Rolle als Bestäuber und Räuber ist. Wenigstens einige Fliegen sind nötig um eine ausreichende Bestäubung zu sichern, aber ein kontinuierlicher Anstieg innerhalb der Blüten hat einen erhöhten Verlust an Samen durch die Larven zur Folge. Daher haben höhere Pflanzendichten einen positiven Effekt auf die per capita Samenproduktion, da sie die Chiastocheta Dichte unabhängig von der gesamten Populationsgrösse verringern.Populationen der Trollblume können derzeit gut in der bereits stark veränderten Landschaft existieren und zeigen bisher keine negativen Auswirkungen der Landschaftszerteilung. Unsere Studie zeigt die Bedeutung einer genauen Betrachtung der Faktoren, die den Fortpflanzungserfolg einer Art bestimmen. Diese sind nicht immer nur die allgemeine Populationsgrösse, sondern können auch andere sein, wie zum Beispiel in diesem Fall Pflanzendichte 2 CHAPTER 1 - INTRODUCTION INTRODUCTION 3 CHAPTER 1 - INTRODUCTION Biodiversity in a changing world For many centuries, human activities have been changing ecosystems and landscapes, and today about one half of the entire global land surface can be considered to be altered by anthropogenic causes (Vitousek et al., 1997, Saunders et al., 1991, Ehrlich and Wilson, 1991). Besides climate change and invasive species, habitat fragmentation caused by human modification of natural landscapes is the main threat to biodiversity and terrestrial ecosystems worldwide (Sala et al., 2000, Fahrig, 2003, Reed, 2004). While biodiversity can be seen as a value in itself, it also has considerable economic value through various services. Indeed, current biodiversity declines have been estimated to be causing economic losses of up to €50 billion each year (Braat et al., 2008). While most of these losses occur in tropical rainforest regions, developed countries are also strongly affected by habitat fragmentation and landscape alteration, often caused by expanding settlement areas, urban sprawl and intensive agriculture (Antrop, 1998, Tilman et al., 2001). In consequence, species extinction rates are now considerably higher than before such widespread landscape and ecosystem alteration (Ehrlich and Wilson, 1991, Thompson and Jones, 1999, Saunders and Briggs, 2002, Hanski and Ovaskainen, 2002, Loreau et al., 2001). Specifically, many regional and local plant extinctions have been caused by direct habitat loss or altered ecosystem processes within and across small and recently fragmented populations (Drayton and Primack, 1996, Fischer and Stöcklin, 1997, Thompson and Jones, 1999, Stehlik et al., 2007). In Switzerland, where urbanization is expanding rapidly (Schulz and Dosch, 2005), wet habitats have undergone especially drastic changes during the last century. Up to 90% of the former wet meadow areas have been lost due to drainage, deterioration and fertilization (Broggi and Schlegel, 1989, Bowman et al., 2008), with many localised plant extinctions (Stehlik et al., 2007, Lienert et al., 2002a, Lienert et al., 2002b, Lienert and Fischer, 2003, Jules, 1998, Hooftman et al., 2003). Habitat
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