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Teixeira De Sousa.Pdf BEHAVIOURAL REGULATION OF MINERAL SALT INTAKE IN THE ADULT WORKER HONEY BEE, Apis mellifera BY RAQUEL TEIXEIRA DE SOUSA A THESIS SUBMITTED IN FULFILMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY IN INSECT BEHAVIOUR & NUTRITION SUPERVISED BY PROFESSOR GERALDINE WRIGHT FACULTY OF MEDICAL SCIENCES INSTITUTE OF NEUROSCIENCE UNITED KINGDOM ii ã 2019 RAQUEL TEIXEIRA DE SOUSA ALL RIGHTS RESERVED iv TABLE OF CONTENTS ABSTRACT xi RESUMO (PORTUGUESE) xiii ACKNOWLEDGEMENTS xix DECLARATION xxiii PREFACE xxv LIST OF TABLES xxix LIST OF FIGURES xxxi LIST OF ABBREVIATIONS xxxiii CHAPTER 1 GENERAL INTRODUCTION AND GOALS 1 1.1 Abstract 3 1.2 Animal NutritiOn – The Necessary Intake Of Nutrients 3 1.3 MacrOnutrients: FunctiOn and Basic Requirements 5 1.4 MicrOnutrients: FunctiOn and Basic Requirements 6 1.4.1 Minerals as Essential Nutrients 6 1.5 IntrOducing the HOney Bee, Apis mellifera 11 1.5.1 Colony Structure of a Superorganism 11 1.5.2 Caste Differentiation 12 1.5.3 Behavioural Maturation and Assessment of Colony Needs 15 1.5.4 Delivering Pollination Services 16 1.6 Source Of Nutrients - Honey Bee FOOd 17 1.6.1 Nectar – Energy Food Source 17 1.6.2 Pollen – Prime Source for Non-Carbohydrates 20 1.6.3 Water – Source for Minerals 25 1.7 HOw DO HOney Bees Taste Nutrients in FOOd? 26 1.8 Mineral NutritiOn in HOney Bees 29 1.9 Bertrand’s Rule. Eating Within the Right Range 32 1.10 Mechanisms Regulating Salt Intake 35 1.11 BehaviOural RegulatiOn Of Nutrient Intake in a SuperOrganism 37 1.12 Significance Of this Study 41 1.13 Study GOals and Specific Aims 43 1.14 Experimental ApprOach. 44 1.15 ROadmap and Structure Of this Thesis 44 CHAPTER 2 OPTIMISATION OF FEEDING ASSAYS: MINERAL RANGE-FINDING, EXPERIMENTAL PROTOCOL AND DATA PROCESSING 47 2.1 Highlights 49 2.2 Abstract 50 2.3 BackgrOund 51 2.4 Study 1. Finding Range That SuppOrts Survival and Testing 53 2.4.1 Study 1. Rationale & Methods 53 2.4.2 Study 1. Results 58 2.4.3 Study 1. Discussion 63 2.5 Study 2. Evaluating EvapOratiOn Rates Inside IncubatOr Chambers 67 2.5.1 Study 2. Rationale & Methods 67 2.5.2 Study 2. Results 67 2.5.3 Study 2. Discussion 69 2.6 Study 3. Testing MethOdOlOgies tO COrrect COnsumptiOn Measurements fOr EvapOratiOn LOss Of Liquid Diets 70 2.6.1 Study 3. Rationale & Methods 70 2.6.2 Study 3. Results 72 2.6.3 Study 3. Discussion 77 2.7 Study 4. Testing the Impact Of Diet Delivery Regime On COnsumptiOn 78 2.7.1 Study 4. Rationale & Methods 78 2.7.2 Study 4. Results 80 2.7.3 Study 4. Discussion 82 2.8 Study 5. Testing the Number Of Bees per Feeding BOx On the Reliability Of ConsumptiOn Measurements 85 2.8.1 Study 5. Rationale & Methods 85 2.8.2 Study 5. Results 86 2.8.3 Study 5. Discussion 90 vi 2.9 ConclusiOn 94 CHAPTER 3 GUSTATORY RESPONSES TO MINERAL SOLUTIONS BY HARNESSED FORAGER BEES 95 3.1 Highlights 97 3.2 Abstract 98 3.3 BackgrOund 99 3.4 MethOds 103 3.4.1 Animal Stocks 103 3.4.2 Animal Collection and Harnessing 104 3.4.3 Animal Preparation and Harnessing for Taste Assays 105 3.4.4 Antennal Stimulation – PER responses 106 3.4.5 Proboscis Stimulation – Drinking Responses 107 3.4.6 Effect of Sucrose Gradient on the Gustatory Perception of Sodium Solutions 108 3.4.7 Solution Stimulus 109 3.4.8 Statistical Analysis 111 3.5 Results 113 3.5.1 Antennal Gustatory Responses to Salts in Solution 113 3.5.2 Antennal Gustatory Responses to Metals in Solution 114 3.5.3 Effect of the Anion Type on the Antennal PER Responses to Metal Solutions 115 3.5.4 Drinking Responses to Salts in Solution 115 3.5.5 Drinking Responses to Metals in Solution 118 3.5.6 Effect of the Anion Type on the Drinking Responses to Metal Solutions 121 3.5.7 Effect of a Sucrose Gradient on the Antennal PER responses to Sodium 124 3.5.8 Effect of a Sucrose Gradient on the Drinking responses to Sodium 126 3.6 DiscussiOn 128 3.6.1 Antennal and Drinking Gustatory Responses to Mineral Solutions Differ in Sensitivity 128 3.6.2 Gustatory responses to minerals are shaped by concentrations but not for all minerals 132 3.6.3 Bees showed limited gustatory responses to increasing concentrations of sodium in solution 135 3.7 ConclusiOn 137 3.8 Acknowledgments 139 CHAPTER 4 SELF-PREFERENCE AND BEHAVIOURAL REGULATION OF MINERAL SALT INTAKE IN YOUNG WORKER BEES 141 4.1 Highlights 143 4.2 Abstract 144 4.3 BackgrOund 145 4.4 MethOds 149 4.4.1 Experimental Animals 149 4.4.2 Chemically-defined Diets 150 4.4.3 Feeding Boxes and Feeding Tubes 151 4.4.4 Feeding Treatments and Conditions 154 4.4.5 Assessing self-preference, daily and total consumption of young worker bees fed mineral diets 157 4.4.6 Testing the effects of mineral diets on the survival and fresh body weight of young worker bees 158 4.4.7 Data Processing and Evaporation Loss Adjustments 158 4.4.8 Statistical Analyses 160 4.5 Results 162 4.5.1 Preference for Mineral Diets 162 4.5.2 Daily Preference for Salt Diets 165 4.5.3 Daily Preference for Metal Diets 168 4.5.4 Effects of salt diets in the feeding responses of young worker bees 171 4.5.5 Effects of metal diets in the feeding responses of young worker bees 174 4.5.6 Effects of mineral diets in water consumption 177 4.5.7 Effects of short-term mineral feeding on the fresh body weight of bees 179 4.5.8 Effects of salt feeding on the survival of young worker honey bees 181 4.5.9 Effects of metal feeding on the survival of young worker honey bees 183 4.6 DiscussiOn 187 4.6.1 Free-flying young adult honey bees self-select mineral diets 188 4.6.2 Young worker bees adjust consumption to avoid mineral intoxication 188 4.6.3 Bees mostly preferred and consumed of Na diets at increasing concentrations 192 viii 4.6.4 Young worker bees show limited behavioural regulation of intake at low zinc and manganese diets, but not at high concentrations 193 4.6.5 Using the Bertrand’s rule principle as a tool to predict optimal mineral intake through behavioural regulation 196 4.7 ConclusiOn 198 4.8 Acknowledgments 199 CHAPTER 5 CONCLUDING REMARKS AND OUTLOOK 201 5.1 Abstract 203 5.2 MOtivatiOn and Main Findings Of this Study 204 5.3 LimitatiOns Of this Study 207 5.4 Gap in the Literature. What we knew sO far 208 5.5 PrOspective WOrk and OppOrtunities 216 5.6 Significance Of this Study and ImplicatiOns 217 5.6.1 Beekeeping Practices and Feed Supplements 218 5.6.2 Pollinators Decline and Bee Stocks 219 APPENDIX A 221 Supplementary InfOrmatiOn: Tables and Figures 223 REFERENCES 241 Literature Cited 243 FINAL NOTE 277 x ABSTRACT HOney bees are impOrtant insect pOllinatOrs, which sOcial existence displays remarkable physiOlOgical and behaviOural traits. These are tightly cOntrOlled by dietary cues. DetectiOn, selectiOn and ingestiOn Of foOd entail the regulatiOn Of nutrient intake that leads tO nutritiOnal hOmeOstasis. This study was mOtivated by the lack Of infOrmatiOn On mineral salt feeding preferences and regulatiOn by adult honey bees. Here, in labOratOry-based assays, I assessed the behaviOural respOnses assOciated with feeding behaviOur Of adult wOrker hOney bees tO eight prevalent minerals in pOllen (K, Na, Mg, Ca, Fe, Zn, Cu, Mn). In Chapter 3, using the classical PrObOscis ExtensiOn Reflex apprOach and drinking assays, I tested the gustatOry respOnses Of fOrager bees tO single minerals in either water Or nectar-like sOlutiOns at fOur levels Of cOncentratiOn. I fOund that fOragers (mixed-age) can detect individual salts/metals mineral salts with respOnses depending On mineral identity. Overall, bees fOund lOw mineral levels in water phagOstimulatOry. But when in sucrOse sOlutiOns, Only high Mg, Fe and Cu were rejected. In Chapter 4, using chOice cohOrts, I tested whether newly-emerged bees preferred a “salty” vs. “unsalty” diet and assessed the effects of single minerals On cOnsumptiOn respOnses and survival Over 6 days. I verified that yOung bees 1) perceived and selected specific minerals in fOOd; 2) shOwed behaviOural regulatiOn Of mineral intake, but nOt all minerals were regulated to the same extent; 3) nOt all minerals acted as phagOstimulants at lOw levels, but were deterrent at sufficiently high levels. This wOrk is one of the firsts tO evaluate gustatOry respOnses of minerals, especially metals, and, tO my knOwledge, the first tO assess the dietary self-selectiOn Of salts and metal nutrients in the context of behaviOural regulatiOn Of intake in adult wOrker hOney bees. The current study lays the grOundwOrk fOr explOring mineral salt requirements, feeding preferences and regulatOry mechanisms Of salt intake in hOney bees. Keywords: Apis mellifera, workers, taste model, Bertrand’s rule, micronutrients, behavioural regulation, self-selection, gustation. xii 1 RESUMO As abelhas são insectOs pOlinizadOres impOrtantes cuja Organização sOcial apresenta aspectOs fisiOlógicOs e cOmpOrtamentais nOtáveis. Estes aspectos, por sua vez, são rigOrOsamente cOntrOladOs pOr estímulOs alimentares externOs. A regulação dO cOnsumO de nutrientes é efectuadO através de mecanismOs de detecção, selecção e ingestão que asseguram a hOmeOstasia nutriciOnal. Um dOs grandes mOtivOs para a realização deste estudO incide sObre a falta de infOrmação existente relaciOnada cOm a ingestão de nutrientes minerais e de que fOrma estes influenciam a cOmpOrtamentO alimentar de abelhas adultas.
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