SCUOLA DI DOTTORATO UNIVERSITÀ DEGLI STUDI DI MILANO-BICOCCA Department of Department of Biotechnology and Biosciences PhD program Life Sciences Cycle XXIX Curriculum in Biology (Morfo-funcional) Aves remores: responses of migratory birds to climate change and habitat alteration Surname: Musitelli Nome: Federica Registration number 072546 Tutor: Dr. Roberto Ambrosini Coordinator: Prof. Marco Ercole Vanoni ACADEMIC YEAR 2016/2017 University of Milano-Bicocca Department of Biotechnology and Biosciences PhD program: Life Sciences – XXIX Cycle Aves remores: responses of migratory birds to climate change and habitat alteration Federica Musitelli Matr. 072546 Academic Year 2016 – 2017 1 Abstract Index Abstract ..................................................................................................... 7 Riassunto ................................................................................................. 10 General introduction .............................................................................. 13 1.1 Bird migration ...................................................................... 14 1.2 Migratory connectivity and seasonal interactions ............ 19 1.3 “Winged sentinels”: impact of environmental conditions on avian migrators .................................................................... 25 1.3.1. Climate change ..................................................................... 26 1.3.2. Environmental changes ....................................................... 32 1.4 Ringing data in the study of bird migration ...................... 35 1.5 Avian microbiomes .............................................................. 39 1.6 Begging behaviour ................................................................ 41 1.7 Thesis structures .................................................................. 43 1.8 Study species ......................................................................... 46 1.8.1. The Barn swallow (Hirundo rustica, Linnaeus 1758) ........ 47 1.8.2. The Common swift (Apus apus, Linnaeus 1758) ............... 51 1.8.3. European robin (Erithacus rubecula, Linnaeus 1758) ...... 54 2 Index PART I ..................................................................................................... 56 Chapter 2 Representing migration routes from re-encounter data: a new method applied to ring recoveries of Barn swallows (Hirundo rustica) in Europe ................................................................................... 57 2.1 Abstract ................................................................................. 59 2.2 Introduction .......................................................................... 61 2.3 Methods ................................................................................. 64 2.4 Results ................................................................................... 74 2.5 Discussion .............................................................................. 93 2.6 Acknowledgments ................................................................ 99 2.7 References ........................................................................... 100 Chapter 3 Environmental conditions at arrival to the wintering grounds and during spring migration affect population dynamics of Barn swallows Hirundo rustica breeding in Northern Italy ............. 106 3.1 Abstract ............................................................................... 107 3.2 Introduction ........................................................................ 109 3.3 Methods ............................................................................... 113 3.4 Results ................................................................................. 125 3.5 Discussion ............................................................................ 128 3.6 Acknowledgments .............................................................. 137 3 Index 3.7 References ........................................................................... 138 Chapter 4 Migratory connectivity and effects of winter temperatures on migratory behaviour of the European robin Erithacus rubecula: a continent-wide analysis ........................................................................ 143 4.1 Abstract ............................................................................... 145 4.2 Introduction ........................................................................ 146 4.3 Materials and Methods ...................................................... 150 4.4 Results ................................................................................. 159 4.5 Discussion ............................................................................ 170 4.6 Acknowledgments .............................................................. 180 4.7 References ........................................................................... 182 PART II ................................................................................................. 186 Chapter 5 Effects of livestock farming on birds of rural areas in Europe ................................................................................................................ 187 5.1 Abstract ............................................................................... 188 5.2 Introduction ........................................................................ 189 5.3 Methods ............................................................................... 193 5.4 Results ................................................................................. 206 5.5 Discussion ............................................................................ 210 5.6 Acknowlegments ................................................................. 215 4 Index 5.7 References ........................................................................... 215 Chapter 6 Cloacal microbiota of Barn swallows from Northern Italy ................................................................................................................ 221 6.1 Abstract ............................................................................... 222 6.2 Introduction ........................................................................ 223 6.3 Methods ............................................................................... 225 6.4 Results ................................................................................. 230 6.5 Discussion ............................................................................ 234 6.6 Acknowledgments .............................................................. 238 6.7 References ........................................................................... 239 Chapter 7 Common swift feather microbiota described by high throughput DNA sequencing ............................................................... 242 7.1 Abstract ............................................................................... 243 7.2 Introduction ........................................................................ 244 7.3 Methods ............................................................................... 246 7.4 Results ................................................................................. 254 7.5 Discussion ............................................................................ 260 7.6 Aknowledgments ................................................................ 263 7.7 References ........................................................................... 264 5 Index Chapter 8 Parent-absent begging in Barn swallow broods: causes of individual variation and effects on sibling interactions and food allocation ............................................................................................... 269 8.1 Abstract ............................................................................... 270 8.2 Introduction ........................................................................ 271 8.3 Materials and Methods ...................................................... 276 8.4 Results ................................................................................. 285 8.5 Discussion ............................................................................ 293 8.6 References ........................................................................... 300 General discussion ................................................................................ 305 Conclusions ........................................................................................... 316 References ............................................................................................. 319 Acknowledgments ................................................................................. 339 Supplementary materials ..................................................................... 340 6 Abstract Abstract Climate change and habitat modification are the main anthropogenic causes of the alarming loss of the worldwide biodiversity. Birds are considered excellent indicators of the consequence of the ongoing global environmental change because they are highly visible due to diurnal lifestyle, mobile, and widespread in almost all habitats. Migratory birds, in particular, are considered particularly sensitive to these changes because they experience divergent patterns of change in ecological conditions in the areas where they spend different phases of their annual life-cycle. The present dissertation investigates the multifaceted effects of climate change and habitat alteration on migratory birds. In particular, it provides empirical evidence of how migrants are affected by and react to variability in the ecological conditions at non-breeding grounds and during migration journeys. First, I propose a novel automatized method for representing migration routes through the analyses of mark-recaptures data. The procedure tested on the Barn swallow ring-recoveries was able to reconstruct patterns of migration consistent with previous knowledge on this species. This study thus discloses the possibility to use the method on other less-studied species and emphasized the often-unexploited informative values of ringing data. Second, I investigate how general ecological conditions (summarized by indices of primary productivity) experienced by Barn swallows in their sub-Saharan non-breeding ranges and during migratory journeys affect the 7 Abstract population dynamic of the species. Results indicate that the arrival at the non-breeding ground and at a key passage area along spring migration route were the most critical phases of the annual life-cycle of this long-distance migrant. In a further study based on ring recoveries, I find that, in the partial migrator European robin, the proportion of individuals that migrate, and the distance travelled by birds from migratory population decrease during milder winter temperatures at the breeding grounds. These studies indicate that environmental conditions during non-reproductive season may strongly affect migratory behaviour of both long and short-distance migrants with significant impact on demographical trends and distributions. Moreover, a degree of variability of phenological responses among populations is observed. Third, through a quantitative meta-analysis of the existing literature, I investigate the effect of livestock farming on farmland birds, a group of birds that are suffering sharp declines in Europe in recent decades. This study confirms that abandonment of livestock has negative effects on Barn swallow abundance and reproduction, but not on other farmland birds. An experimental test of food deprivation on Barn swallow nestlings further confirms that resources availability at breeding sites can alter nestling begging behaviour and intra-brood interactions with potential consequences on their quality. Finally, I contribute to the characterization of the gut microbiome of the Barn swallow and of the plumage bacteria of the Common swift. 8 Abstract Results suggest that studies of bird microbiomes, despite they are still in their infancy, may be relevant for investigating the ecology of migration. 9
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