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Bumblebee Ecophysiology: Assessing the Impacts of Climate Change and Pesticide Use on Bombus Terrestris Audax and B

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Bumblebee Ecophysiology: Assessing the Impacts of Climate Change and Pesticide Use on Bombus Terrestris Audax and B BUMBLEBEE ECOPHYSIOLOGY: ASSESSING THE IMPACTS OF CLIMATE CHANGE AND PESTICIDE USE ON BOMBUS TERRESTRIS AUDAX AND B. T. DALMATINUS By Emily Louise Owen A thesis submitted to The University of Birmingham for the degree of DOCTOR OF PHILOSOPHY School of Biosciences The University of Birmingham October 2014 University of Birmingham Research Archive e-theses repository This unpublished thesis/dissertation is copyright of the author and/or third parties. The intellectual property rights of the author or third parties in respect of this work are as defined by The Copyright Designs and Patents Act 1988 or as modified by any successor legislation. Any use made of information contained in this thesis/dissertation must be in accordance with that legislation and must be properly acknowledged. Further distribution or reproduction in any format is prohibited without the permission of the copyright holder. ABSTRACT Climate change is altering the phenology of bumblebees in parts of the UK, with worker activity recorded during winter. This presents a unique set of physiological challenges to bumblebees, as they are typically exposed to exclusively summer conditions. The aim of this thesis was to assess the capacity for winter activity and survival in the UK-native bumblebee Bombus terrestris audax (Harris, 1780) (Hymenoptera: Apidae) and the commercially- imported B. t. dalmatinus Dalla Torre, 1882 (Hymenoptera: Apidae). Cold tolerance assessments indicated that both subspecies were physiologically ill-adapted to winter temperatures. However, both species were found to undergo Rapid Cold Hardening (RCH); the first evidence of RCH in Hymenoptera. Thermal activity thresholds (CTmin, chill coma and chill coma recovery) were significantly lower in B. t. audax than B. t. dalmatinus. However, only B. t. dalmatinus was able to lower these thresholds as a result of acclimation. This highlights the potential for competition between the subspecies. Field experiments showed a lack of winter-active bumblebees in Birmingham, and an inability of commercial colonies to survive winter. Finally, this thesis presents the first evidence to suggest that sub- lethal neonicotinoid exposures impair bumblebee activity at low temperatures. Results are discussed in the light of climate change, pesticide use and the bumblebee pollinators in future climate scenarios. ii “Every kid has a bug period... I never grew out of mine.” E. O. Wilson. iii ACKNOWLEDGEMENTS I would like to thank: the BBSRC for funding this project, BioBest for supplying the bumblebees and Agralan for shipping them to the UK. My thanks also go to Winterbourne Botanical Gardens, for allowing me to carry out field experiments in their grounds. I would also like to thank Tom Ings, whose advice on bumblebee biology and handling was invaluable, especially in setting up my own bumblebee lab. I am lucky to have received exceptional supervision throughout my PhD, from Scott Hayward and Jeff Bale. I am extremely grateful to Scott for his continued support throughout the course of my PhD. From the creation of a bumblebee lab to the end of my thesis write-up, his door has always been open, and no question was too silly! I would like to thank Jeff Bale, for welcoming me into his lab as an undergraduate, and again as a PhD student. I am grateful for the guidance he has given me over the years, and I have enjoyed listening to his excellent stories during lab outings. There was never a dull moment in the Arthropod Ecophysiology lab. Special thanks to Megan, Nicky and Matt for our cake and coffee outings, to Bobbie and Paul for our stupid games and to Dec for his much-needed company. Thanks also to Gwen, Lucy, Stuart and Ji, who welcomed me both as an undergraduate and as a PhD student to the lab, and provided support and guidance throughout my time at Birmingham. Thanks to my many mad friends, who have provided an endless source of fun, beer and bee jokes. Thanks also to my family, who now know more about bees than they ever wished to know. Special thanks to my Mom and Dad, who have provided me with support and encouragement throughout my academic career. I could not have done it without you. Finally, thanks to Jon who has kept me sane(ish) throughout the past 10 years, and has proven himself as an all- round brilliant human being. iv TABLE OF CONTENTS CHAPTER 1 Introduction ...................................................................................................... 1 1.1. Insect-environment interactions in a changing climate ....................................... 1 1.2. Insect cold tolerance ............................................................................................ 5 1.3. Experimental measures of cold tolerance .......................................................... 15 1.4. Effects of acclimation on cold tolerance ........................................................... 19 1.5. Overwintering strategies in a seasonal climate ................................................. 23 1.6. Insect pollination ............................................................................................... 28 1.7. Bumblebees in agriculture ................................................................................. 28 1.8. Bombus terrestris: life cycle .............................................................................. 30 1.9. Bombus terrestris: diapause .............................................................................. 32 1.10. Bombus terrestris: thermoregulation ............................................................... 34 1.11. Bombus terrestris: subspecies ......................................................................... 37 1.12. Bombus terrestris in the UK: B. t. audax and B. t. dalmatinus ....................... 39 1.13. Winter active bumblebees ............................................................................... 40 1.14. Pesticides and agriculture ................................................................................ 41 1.15. Neonicotinoids ................................................................................................. 42 1.16. Negative impacts of neonicotinoids ................................................................ 44 1.17. Thiacloprid ...................................................................................................... 46 1.18. Thesis structure ................................................................................................ 48 1.19. Thesis aims ...................................................................................................... 51 CHAPTER 2 Can winter-active bumblebees survive the cold? Assessing the cold tolerance of Bombus terrestris audax and the effects of pollen feeding ............................. 52 2.1. Abstract.............................................................................................................. 52 v 2.2. Introduction ....................................................................................................... 53 2.3. Methods ............................................................................................................. 58 2.4. Results ............................................................................................................... 63 2.5. Discussion.......................................................................................................... 71 CHAPTER 3 Can non-native bumblebees survive UK winters? Establishment risk of the commercially-imported Bumblebee Bombus terrestris ....................................................... 76 3.1. Abstract.............................................................................................................. 76 3.2. Introduction ....................................................................................................... 77 3.3. Methods ............................................................................................................. 80 3.4. Results ............................................................................................................... 84 3.5. Discussion.......................................................................................................... 88 CHAPTER 4 Bumblebee activity in a changing climate: thermal activity thresholds of native (Bombus terrestris audax) and non-native (Bombus terrestris dalmatinus) bumblebees ............................................................................................................................. 95 4.1. Abstract.............................................................................................................. 95 4.2. Introduction ....................................................................................................... 96 4.3. Methods ........................................................................................................... 101 4.4. Results ............................................................................................................. 105 4.5. Discussion........................................................................................................ 114 CHAPTER 5 Phenology of wild B. t. audax in Birmingham and the capacity for winter colony survival ..................................................................................................................... 122 5.1. Abstract............................................................................................................ 122 5.2. Introduction ....................................................................................................
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