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Impacts of Ozone Pollution on Nectar and Pollen Quality and Their Significance for Pollinators

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Impacts of Ozone Pollution on Nectar and Pollen Quality and Their Significance for Pollinators IMPACTS OF OZONE POLLUTION ON NECTAR AND POLLEN QUALITY AND THEIR SIGNIFICANCE FOR POLLINATORS Daniel Stabler A thesis submitted for the degree of Doctor of Philosophy School of Biology Newcastle University April, 2016 i I hereby declare that this thesis is based on work conducted by myself and has not contributed to any other degree. Reference to ideas and work of others has been specifically acknowledged. ii Abstract This thesis explores the impacts of ozone pollution on the nutritional quality of nectar and pollen. We report the use of HPLC and HPIC to quantify the amino acids and carbohydrates in nectar and the development of a microwave-assisted acid hydrolysis to quantify the protein- bound amino acids available in pollen, allowing back-calculation to estimate total protein content. Utilising ten cultivars of broad bean (Vicia faba L.), exhibiting considerable variation in response to ozone, we explored what parameters are meaningful when attempting to determine the impacts of ozone (reductions in biomass, seed yield etc.) and whether these measures are consistent with the influence of the pollutant on pollen quality. We found little correlation between impacts on pollen quality and any usually-measured plant traits affected by ozone. We concluded that ozone influences pollen qualities in two ways; (i) exposure to ozone during plant growth influences the allocation of proteins to pollen, and (ii) ozone may cause direct oxidative damage to pollen once dehisced from anthers. We investigated the impact of ozone on the allocation of amino acid and carbohydrate resources to nectar and pollen, using broad bean (Vicia faba L.) as a convenient model. Plants grown in O3 and exposed to charcoal/purafil® filtered air (CFA) at flowering allocated significantly more sucrose and amino acids into their nectar than plants in other fumigation treatments. We discovered a reduction in the amount of free amino acids recoverable from the outer surface of the pollen in all treatments subject to O3 exposure, but most significant in plants maintained throughout in O3. We also found a significant shift in the proportions of amino acids in the respective ozone treatments. The final experimental thesis chapter explored the potential impact of ozone-induced changes in nectar quality on bee behaviour. Simulated ozone-induced changes in nutrient composition of nectar were employed in an olfactory conditioning assay using honeybees. Bees trained with nectar matching that of plants subject to O3 and exposed to CFA at flowering demonstrated an initially improved rate of learning, but association with reward decreased rapidly, whereas those trained with nectar matching that of plants from CFA was sustained. iii Acknowledgements Firstly, I wish to thank my committed and always supportive (with the odd put- down to keep me in check) supervisors, Prof Jerry Barnes and Prof Jeri Wright. You have both offered me endless encouragement and I am sincerely grateful to you both. It looks like you’ll be stuck with me for a few more years too! There are countless people who deserve thanks for contributing time, effort and support to my work presented in this thesis: Alan Craig, I simply couldn’t have carried- out my ozone experiments without you and I apologise for the constant phone calls seeking your help with ozone experiments. Thank you to Dr. Kirsten Wyness for her help with experiments in the open top chambers. Alexandria McCallum, for never complaining about moving hundreds of broad beans around Close House with me; rain or shine! Kerry Simcock, I know I’m still not forgiven for the days of root-washing but I am truly grateful for your help. Thank you also for your help with bee feeding experiments. Damien Charriere, never have I met a man with such patience and determination with a fine balance. You saved my sanity by providing assistance in the weighing-out of thousands of pollen samples. Gemma Kitson, thank you for never giving up when Bradford standard curves were just not good enough. Thank you to Dr. Eileen Power for showing me the ropes with HPLC and then promptly leaving the country. I should have noticed it was a warning! To all members of the bee lab and the EMPP group, past and present, thank you for the years of laughter and allowing me to vent my rage at the HPLC. I’d like to give a special mention to Helen Gray and Kerry Simcock. Quite simply two of the most ridiculous people I have ever met. Thank you for your constant entertainment and giving back just as much sass as I give. To my family. For some ungodly reason I was blessed with a delightful bunch of you. I couldn’t have done this without you. My biggest thank to all of you is for your spectacular sense of humour. May the laughter continue! Mam and Dad, Pauline and Dave, I will probably never be able to repay you in the love, support and yes, money, that you’ve devoted on me over the last 27 years. Thank you for absolutely everything. But most importantly thank you for encouraging me to do what I wanted to do. Finally, to my baby angel squish of a dog, Pup, thank you for keeping me sane (ish). iv Table of Contents Thesis title ..................................................................................................................... i Declaration ................................................................................................................... ii Abstract ....................................................................................................................... iii Acknowledgements ..................................................................................................... iv Abbreviations .............................................................................................................. ix Chapter 1: General introduction ................................................................................ 1 1.1 Background to ozone .............................................................................................. 1 1.2 Ozone formation and distribution ......................................................................... 2 1.3 Ozone phytotoxicity and plant responses ............................................................. 4 1.4 Risks posed by ozone to agriculture ...................................................................... 5 1.5 Impacts of ozone on plant reproductive processes ............................................... 6 1.5.1 Nectar ............................................................................................................. 7 1.5.2 Pollen ............................................................................................................ 10 1.6 Pollinators ............................................................................................................ 11 1.7 Project outline ...................................................................................................... 13 Chapter 2: Exploration of methods to quantify the amino acid qualities of pollen ... 15 2.1 Introduction ......................................................................................................... 15 2.2 Methods .............................................................................................................. 19 2.2.1 Pre-treatment regimes: Estimation of protein content of pollen ................. 19 2.2.2 Efficacy of Bradford assay with different proteins ........................................ 20 2.2.3 Impact of protein hydrolysis on Bradford assay ........................................... 20 2.2.4 Optimisation of protein hydrolysis for HPLC analysis ................................... 20 2.2.5 Optimisation of pollen protein hydrolysis ..................................................... 21 2.2.6 Amino acid analysis ...................................................................................... 22 2.2.7 Statistical analysis ........................................................................................ 23 2.3 Results ................................................................................................................. 24 2.3.1 Pre-treatment regimes: Estimation of protein content of pollen ................. 24 2.3.2 Efficacy of Bradford assay with different proteins ........................................ 25 2.3.3 Optimisation of pollen protein hydrolysis ..................................................... 25 2.3.4 Protein-bound amino acids – low weights .................................................... 28 2.3.5 Free amino acids – low weights .................................................................... 29 2.3.6 Protein-bound amino acids – higher weights ............................................... 30 2.3.7 Free amino acids – higher weights ............................................................... 30 2.4 Discussion ............................................................................................................ 33 2.4.1 Estimation of protein concentration from amino acids in pollen hydrolysate ................................................................................................................................ 33 2.4.2 Protein Quantification using a Bradford assay depends on solubility of the protein .................................................................................................................... 36 2.4.3 Free amino acids are reliably measured in pollen weights ≥ 1 mg ............... 37 2.4.5 Conclusion ....................................................................................................
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