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The Nutritional Ecology of Farmland Bees: A The Nutritional Ecology of Farmland Bees: a Behavioural & Community Approach Alexander James Austin Department of Biological & Marine Sciences University of Hull MSc. Conservation Biology - University of Plymouth BSc. (Hons) Marine Biology - University of Plymouth A thesis submitted for the degree of Doctor of Philosophy May 2019 For the fathers I lost. I miss you both more than I can express. I am the man you made me, and so this is for you. 1 “Other kings said I was daft to build a castle on a swamp, but I built it all the same, just to show ‘em. It sank into the swamp. So, I built a second one… that sank into the swamp. So, I built a third… that burned down, fell over, and then sank into the swamp. But the fourth one... stayed up” Michael Palin as the King of Swamp Castle, Monty Python and the Holy Grail 2 Acknowledgements Firstly, I would like to thank my primary supervisor Dr. James Gilbert and my co- supervisor Dr. Lori Lawson-Handley. I would like to say a particularly sincere thank you to James. After being inherited as James’ PhD student I at first felt somewhat discarded, but my fears of being an unwanted attaché were unfounded. James has not only offered unwavering support and advice across this diverse and challenging project, but has always treated me like a colleague and a valued collaborator, something that is all too rare. More than that however, he has given me my confidence back; a level of self-belief that I thought I had lost. That is something I consider priceless and is a debt I cannot repay. I am immensely proud to have been his first PhD student. Lori, also, has been of great support to me during my time at Hull, she stepped up to be my co-supervisor when she did not have to, whilst also having other PhD students to supervise. Lori went above and beyond in that regard and for that she has my continuing gratitude. Of those at Hull University there are a handful of others, outside of my supervisors, who I would also like to give a special thanks to, and without whom I would not have made it this far. A big and special thanks to Graham Sellers, who not only took me under his wing and taught me everything I know about DNA extraction, but was also a great friend throughout my PhD. Thanks for all the coffee (although I do blame you for my mild caffeine addiction) and chats that have kept me sane - which is one hell of an achievement by the way - and all the other laughs, trolls, shamblers and hot shoes. Another big thanks to Marco Benucci, without whom I would have surely lost my mind during the bioinformatics analysis. Thank you for enduring my unending questions, my constant badgering, my sometimes uncontrollable “Blackaddery” attitude, and for just getting me. I’d also like to 3 thank Tom Evans for being an all-around good mate and for being another cardboard- comprehensive school kid like me. A final quick thanks to Dr. Rob Donnelly who is unfailing in his support of all the PhD students, myself very much included, and has never once been too busy to help, even when he really is. I have enjoyed working with all the people in the department, it has a true familial atmosphere and a genuine ethos of support and collaboration irrespective of field, something that I think is very rare indeed. I hope that I can find something like that again when I leave Hull. I have also had so much support outside of the university from my family, who have always believed in me, even when I did not. To my mum Julia, who’s weekly trips to the library, willingness to turn a blind eye to my staying up late to watch Wildlife on One, and fervent belief that a person can be successful irrespective of their background, undoubtedly laid the foundations for me reaching this stage. Thanks mum, for your unwavering belief and for giving me ambition. To my Dad Alec, you taught me that nothing worth having in life is easy to attain, I owe my work ethic, my moral character, and my stubborn unwillingness to stay down to you. I could not have done this without the courage you taught me. Going on without you at my back is the hardest thing I have ever had to contemplate, but you made me strong and I shall ever endeavor to make you proud. To my Nan and Pap, who were as much parents to me as anyone, thank you for being the most loving, kind, genuine, and selfless role-models a grandson could ask for, not just through this but through my entire life. You are the greatest people I have ever known. Last, but by no means least, I want to give the most heartfelt thanks of all to my wife Claire. You have been my rock, my confidante, my best friend and my greatest believer. Your love and support has often been the only thing that has kept me going during this PhD, and I can 4 honestly say I would never have achieved it without you by my side. Thank you for helping me to the second greatest achievement of my life. 5 Abstract Nutritional degradation, attributed to agriculture, is a primary driver of bee declines, yet we know very little about bee larval nutrition. How larvae deal with nutritional variation in their provisions remains relatively unexplored. Additionally, the nutritional requirements of adult and larval bees differ, yet such a distinction is rarely considered when investigating bee-flower communities. Using the Geometric Framework I ask (a) whether solitary bee larvae (Osmia bicornis) regulate their nutrient intake, and (b) whether the importance of macronutrients change across development. Second, I investigate (a) how bee and host plants communities change within a flight season on organic and conventional farms, and (b) how bees’ foraging decisions shape their interaction networks. Specifically, using DNA metabarcoding of pollen, I separate larval- and adult-focussed foraging interactions. I show that larval bees prioritise carbohydrate over protein, but that the importance of individual macronutrients shifts from protein to carbohydrate throughout development. I also demonstrate that larvae regulate lipid intake, a macronutrient often overlooked in bee nutrition. I show that organic farms support higher abundances, but not higher diversity, of plants and bees, and that nutritional resources vary more with season than farming practice. Lastly, I show that bees forage differentially for their offspring, highlighting the need to consider both adult and larval nutrition when managing landscapes for bees. These findings highlight the importance of a holistic view of bee nutrition. Larval bees are able to regulate their nutritional intake, suggesting a capacity to deal with nutritional variation. However, this ability is limited, with bees perhaps being vulnerable to undetectable changes to their nutritional environment. Nutritional resources also differ phenologically across farming practices, highlighting the need to address key nutritional 6 gaps for bees. Finally, understanding that bee parental care shapes the way bees interact with their environment is essential to providing quality floral resources that address both adult and larval needs. 7 Contents 1. Introduction 1.1. Bees: a brief background…………………………….….….………..….…10 1.2. Multiple threats, bees in decline ……………………………………….….14 1.3. Osmia bicornis, the Red Mason bee ………………………………………17 1.4. Pollen, bees, and their nutrional interactions ………….…………………..20 1.5. Chapters of this thesis ……………………………………………………..26 2. The geometry of dependence: bee larvae prioritise carbohydrate over protein in parentally provided pollen 2.1. Abstract …………………………………………………….….….……….34 2.2. Introduction ……………………………………………………..…………36 2.3. Methods ………………………………………………………………...….40 2.4. Results ……………………………………………………………..………48 2.5. Discussion …………………………………………………………...…….58 2.6. Supplementary materials ……………………………………………..……66 3. Nutritional needs and preferences of solitary bee larvae shift during development 3.1. Abstract ……………………………………………………………...…….70 3.2. Introduction ……………………………………………………………..…72 3.3. Methods ……………………………………………………………………75 3.4. Results ………………………………………………………………..……80 3.5. Discussion ……………………………….….….….…….….…….……….95 8 3.6. Supplementary materials …………………………………………..……103 4. Plugging the hunger gap: Organic farming supports more abundant nutritional resources for bees at critical periods 4.1. Abstract …………………………………………..………………...….…107 4.2. Introduction ……………………………………………………….……...109 4.3. Methods …………………………………………………………………..112 4.4. Results ……………………………………………………………………116 4.5. Discussion ………………………………………………..………………125 4.6. Supplementary materials …………………………………………………133 5. As mother says not as mother does: bees forage differentially for themselves and for their offspring 5.1. Abstract ……………………………………………………………..……139 5.2. Introduction ………………………………………………………………141 5.3. Methods ……………………………………………………..……………145 5.4. Results ……………………………………………………………………151 5.5. Discussion ………………………………………………..………………164 5.6. Supplementary materials …………………………………………………172 5.6.1. Pollen DNA metabarcoding workflow ….….….…………………172 5.6.2. Supplementary Results ………………………….….…….………182 6. Discussion ………………………………………………………………..………226 7. References ……………………………………………………….……….………233 9 1. Introduction 1.1. Bees: a brief background Bees are a group of Aculeate Hymenopteran insects, a group also including ants and wasps. Widely believed to have originated from wasps (Danforth et al., 2013), bees have switched from a carnivorous lifestyle to one that involves the collection of pollen and nectar from flowers (Falk, 2015). Bees are an often studied group yet, in general, bees are frequently viewed through the lens of common species (Goulson and Nicholls, 2016), such as honeybees and bumblebees, with much of the work studying bee declines being in these groups (Connop et al., 2010; Durant, 2018; Hayes et al., 2008; Kovács-Hostyánszki et al., 2019; Szabo et al., 2012; Williams et al., 2009). However, bees as a group are actually highly varied and speciose (Danforth et al., 2013), with varying morphology, life histories and feeding habits (Falk, 2015; Michener, 2000). In terms of their lifestyles bees can be highly variable yet can be roughly grouped into two classes, solitary and social (Falk, 2015); although this is a continuum as some bees can be facultatively social (Smith et al., 2018, 2019) i.e.
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