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Urban Bees: Reproductive Success, Colony Health and Foraging in an Anthropogenic Environment

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Urban Bees: Reproductive Success, Colony Health and Foraging in an Anthropogenic Environment Urban bees: reproductive success, colony health and foraging in an anthropogenic environment Thesis submitted for the degree of Doctor of Philosophy (PhD) Royal Holloway, University of London March 2019 Ash Edwyn Samuelson Author declaration I declare that all work is entirely my own, except for in the following cases. In Chapter Three and Four, the “creating a land cover map” part of the land classification process for 30 out of 38 sites was performed by a research assistant (Alexis Gkantiragas). In Chapter Five, the Nosema screens were carried out jointly by myself and a technician (Kel Lui). In Chapter Four, the ground surveys of agricultural sites were performed by a research assistant (Maggie Fitzherbert). In Chapter Six, 31% of waggle dances were decoded by nine research assistants and the R code for land-use preference analysis was written collaboratively by myself and Dr Roger Schürch (Virginia Tech). For all chapters, manuscripts were commented on by all named authors. 2 Acknowledgements I am extremely grateful to my supervisors, Elli Leadbeater and Rich Gill, for supporting me through the successes and difficulties during my PhD and particularly to Elli for going above and beyond the duties of a supervisor and allowing me to turn up in the middle of the night to store dead bees in her freezer. I am also very grateful to Mark Brown for acting as an informal supervisor and giving me invaluable guidance both on bumblebee research and academic life in general. I have been fortunate to have a supportive and collaborative group of colleagues in the Leadbeater and Brown labs: particular thanks go to Callum Martin, Harry Siviter, Judy Bagi, Arran Folly, Emily Bailes, Dylan Hodgekiss, Gemma Baron, Dara Stanley, Fabio Manfredini, Chris Pull, Matt Hasenjaeger, Romain Willemet and Gregoire Pasquier, and Steve Portugal and Sarah Papworth from outside the lab. A special thanks to Harry and Judy for helping me feel comfortable to be myself at work. All of the research in this thesis was made possible through collaboration with beekeepers and garden owners, to whom I am extremely grateful for accommodating me taking samples from their hives, placing bumblebee colonies in their gardens and checking them at night and constructing sheds in their apiaries to house observation hives (and for the hundreds of cups of tea!). The many undergraduate project students, Nuffield A-level students and volunteers that assisted with dance decoding and lab work and accompanied me on site visits helped make the workload more manageable and considerably more enjoyable. I am also very grateful to Maggie Couvillon and Roger Schürch for collaborating on the waggle dance work and for giving me the foundations to pursue honeybee research. I am grateful to my funders, the BBSRC, High Wycombe Beekeepers’ Association and Essex Beekeepers’ Association, for making this PhD possible. Thanks also go to IUSSI NW Section for providing funding to attend conferences, and the Crown Estate for allowing collection of bumblebee queens in Windsor Great Park. Particular thanks go to family and friends for their support over the last few years: my brother Joey Samuelson, for helping me construct bumblebee nest boxes and for providing a retreat from PhD work in the form of building projects; my parents for always being there for me and encouraging my interests, and my wonderful London community (especially the writing retreat gang). Special thanks to Hazel for the shared hours working on our respective PhDs together and to Hazel, Max and Herc for providing a safe and supportive home during the final push. 3 Abstract Bees are extremely important pollinators but are under threat from reduction in forage availability, parasites and disease and pesticide exposure. Urbanisation is a rapidly expanding driver of land-use change that is likely to interact with these threats, but it is unclear whether urban areas support or impair bee populations. While there is evidence that the abundance and diversity of bee species may be higher in urban areas, it is not known whether this is driven by effects of land-use on reproductive success or migration, and which mechanisms are behind these effects. This thesis employs a colony-level approach to investigating the effects of urbanisation on honeybees and bumblebees. I first developed a land classification protocol to analyse land-use attributes at a resolution relevant to pollinator use of the landscape. Using this protocol, I investigated bumblebee colony success in city, village and agricultural sites by placing lab-reared colonies of Bombus terrestris into the field and monitoring their development. I found reduced reproductive output, colony size, longevity and queen survival in colonies in agricultural areas. These colonies were also less likely to contain pollen and nectar stores. Building on these findings in wild bees, I investigated the effect of urbanisation on honeybee pollen foraging and colony health by sampling 51 beehives located across a gradient of urbanisation in South-East England in the spring and autumn. Here I found increased pollen species richness, larger colony sizes and lower Nosema infection in colonies located in urban areas. These results in honeybees and bumblebees suggested forage availability may play an important role in mediating the relationship between urbanisation and colony success. To investigate differences in forage availability between urban and rural areas I decoded waggle dances performed by honeybees in ten urban and ten rural sites across an entire foraging season. Urban bees showed consistently lower foraging trip distances, suggesting higher forage availability. This was not compensated for by differences in nectar sugar content, with urban bees collecting nectar with a higher average sugar content than rural bees. Analysis of land-use preferences highlighted the role of residential areas containing gardens in the city and the reliance on mass-flowering crops in the countryside. The results of this thesis suggest that bees are able to thrive in urban areas, and serve to highlight the poor suitability of agricultural land to provide habitat resources for bees and other pollinators. 4 Table of Contents Chapter One: Introduction .................................................................................................................... 13 Bees: ecology and conservation ........................................................................................................ 13 Effects of urbanisation on bees ......................................................................................................... 15 Urban drivers of bee ecology ............................................................................................................ 18 Conclusions and research gaps ......................................................................................................... 24 Summary of research chapters .......................................................................................................... 26 Chapter Two: Methodology .................................................................................................................. 28 General approach .............................................................................................................................. 28 Animal husbandry ............................................................................................................................. 33 Field techniques ................................................................................................................................ 34 Lab techniques .................................................................................................................................. 41 Statistical techniques ......................................................................................................................... 43 Concluding remarks .......................................................................................................................... 44 Chapter Three: A land classification protocol for pollinator ecology research: an urbanisation case study .............................................................................................................................................................. 44 Abstract ............................................................................................................................................. 45 Introduction ....................................................................................................................................... 46 Methods ............................................................................................................................................ 50 Results ............................................................................................................................................... 58 Discussion ......................................................................................................................................... 63 Supplementary Material .................................................................................................................... 69 Chapter Four: Lower bumblebee colony fitness in agricultural compared to urban environments ...... 73 Abstract ............................................................................................................................................. 74 Background ......................................................................................................................................
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