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Reproductive Behaviour of Tetragonula Carbonaria

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Reproductive Behaviour of Tetragonula Carbonaria Native bees as alternative crop pollinators: Reproductive behaviour of Tetragonula carbonaria Francisco Garcia Bulle Bueno School of Life and Environmental Sciences New South Wales, 2006, Australia 2021 A thesis submitted in fulfilment of the requirements of the degree of Doctor of Philosophy Native bees as alternative crop pollinators: Reproductive behaviour of Tetragonula carbonaria Copyright © 2021 Francisco Garcia Bulle Bueno This document is typeset in Times New Roman. R code, plots and tables were in RStudio, I Author Attribution The work contained in the body of this thesis, except otherwise acknowledged, is the result of my own investigations. Chapter 2 is being prepared for submission. Francisco Garcia Bulle Bueno (FGBB) collected and analysed the data. The co-authors of this study are Liam Kendall (LK), Denise Alves (DA), Tanya Latty (TL), Tim Heard (TH), Manuel Lequerica (ML), Ben P. Oldroyd (BPO) and Rosalyn Gloag (RG). All co-authors contributed to the study design. LK, DA and ML contributed to collection of the data. RG, LK, TH and DA provided valuable feedback and editing. Chapter 3 is being prepared for submission. FGBB designed and conducted the experiment. The co-authors of this study are Bernardo Garcia Bulle Bueno (BGBB), Gabriele Buchmann (GB), TH, TL, BPO, Anette Hosoi, (AO) and RG. BGBB assisted in coding and data analyses. GB assisted in the lab work. RG assisted in the experimental design. All authors provided valuable feedback and editing. Chapter 4 is published in Journal of Experimental Biology. FGBB designed and conducted the experiment. The co-authors of this study are Isobel Ronai (IR), TL and RG. All authors provided valuable feedback and editing. Chapter 5 is being prepared for submission. FGBB designed and conducted the experiment. The co-authors of this study are Rabia Hajjar (RJ), Théotime Colin (TC), GB, TL, TH, BPO and RG. RJ assisted in the experimental design and the collection of data from the virgin queens. TC assisted in coding and data analyses. GB assisted in the lab work. All authors provided valuable feedback and editing. Chapter 6 is being prepared for submission. FGBB designed and conducted the experiment. The co-authors of this study are Malcolm Possell (MP), Guillaume Kerdoncuff (GK), GB, TL, TH, and RG. MP assisted in the experimental design and chemical data analyses. GK assisted with the data collection. GB assisted in the lab work. All authors provided valuable feedback and editing. II Preface The chapters presented in this thesis are written in a format for publication in peer-reviewed, scientific journals. For organisation purposes, all references have been compiled at the end of this thesis for easier cross-referencing. This thesis has been saved in a PDF format file and has been submitted digitally. I have made hyperlinks throughout the document for the table of contents, chapters, figures and tables. The links have been coloured in green. Clicking on any section will automatically bring the reader to the relevant chapter, figure or table. Hereafter, I wish these small details will be useful for the reader to better navigate this thesis. III Statement of Authorship This thesis has not been submitted for any other degree or purposes. I certify that the research described in this thesis is the original work of the author, and that all the assistance received in preparing this thesis and sources have been acknowledged. Francisco Garcia Bulle Bueno | 20 December, 2020 As supervisor for the candidature upon which this thesis is based, I can confirm that the authorship attribution statements above are correct. Ros Gloag | 20 December, 2020 IV Acknowledgements This thesis is the product of an amazing support and guidance from very talented and dedicated people which I will acknowledge hereafter. I want to thank my main supervisor Rosalyn Gloag for all her guidance, support and mentorship throughout my PhD. I could not have asked for a better supervisor. Thank you for sharing your passion and enthusiasm for bees and biology, it is contagious. Tim Heard. Thank you for your guidance, support, generosity and help. You opened the door to me of the marvellous world of Australian stingless bees to me and I could not be more grateful for that. I could not have asked for a better conference travel partner for Brazil and the Philippines. I deeply enjoyed our science chats when hiking in the tropics. Tanya Latty. Thank you for the encouragement, cheerful personality and optimism, especially when the experiments did not go as expected. Ben Oldroyd. Thank you for letting me be part of the BEE LAB, the chats about bees and feedback on this work. Gabrielle Buchmann. Thank you for training me and helping me in the lab and the molecular sections of my research. I will always remember the dinners and the chats outside of the lab, as well as your kindness and generosity. Julianne Lim. Thank you for your personal approach and always checking on the PhD students and asking about our life and personal relationships plus the support and help in the fieldwork preparation. Eliza Middleton. Thank you for your unconditional help, friendship and support. V To my fabulous co-authors and volunteers, specially to my brother Bernardo Garcia Bulle Bueno, Isobel Ronai, Théotime Colin and Liam Kendall. Thank you for your time investment and dedication to this thesis, your valuable input in the data analyses and providing excellent feedback to the manuscripts. Liz Gibson, Peter Clark, Lindy Williams and Alex Austin for facilitating the use of colonies of stingless bees from Ku Ring Gai for my fieldwork and training. BEE Lab and the Invertebrate Behaviour and Ecology Lab colleagues. Amanda Norton, Patsavee Utaipanon, Manuel Lequerica, Arisa Hosokawa, Thomas Gillard, Thomas Hagan, Sarah Aamidor, Michael Holmes, Inez Vlasich, Jules Smith and Riley Fergusson. I am very happy and grateful to have walked this PhD path together, for your help and support during times of stress but mostly for the laughs and chats in the student office. Giovanna Lescale for being there in the last months of my PhD, for her love and unconditional support. To my friends and family, the ones in Mexico and the ones in Australia (Daniela Méndez, Rebeca Durán, Isabella Mangos and Grace Barrand). Thank you for the shared memories during my PhD and for making my time in Australia such a joy. Financial support and funding. This thesis would not have been possible if it was not for the University for Sydney and Agrifutures funding. Finally, this thesis is dedicated to my parents for their unconditional support since the moment I was born. VI Abstract Bee pollination benefits the productivity of a wide variety of vegetable and fruit crops worldwide. Although the western honey bee Apis mellifera is the dominant pollinator of most crops, global instability in honey bee populations has led to calls to diversify the world’s pollination services by enlisting other bee species as alternative pollinators. The stingless bees (Meliponini) are top candidates for this role. Like honey bees, they are highly eusocial, and can be managed and propagated in wooden hives. They have a large native distribution covering the tropics and subtropics of the world and are already known to be effective pollinators of many tropical fruits. Knowledge of how to maintain stingless bees in agricultural landscapes will also have substantial benefits for their conservation in the wild, where they provide key ecosystem services to native plants. An important step towards better utilising these bees as crop pollinators is to advance our understanding of their reproductive and foraging biology. In this thesis, I review the plants visited by stingless bees around the world, to uncover broad patterns in their floral visitation (Chapter 2). I then investigate the reproductive biology of the Australian endemic stingless bee Tetragonula carbonaria to: determine the distance males travel between their natal nest and mating aggregations, and assess the viability of using male dispersal behaviour to estimate the colony density of a region (Chapter 3); describe the reproductive anatomy of queens and workers, and confirm that workers are irreversibly sterile as adults (Chapter 4); document the early phase of a queen’s life, and rear and mate queens under controlled conditions (Chapter 5); describe the volatiles produced by virgin queens, males and queenless colonies, and assess their effect on the attraction of rival colonies (Chapter 6). Together, these new insights improve our understanding of the biology of T. carbonaria and other stingless bees, and bring us closer to the goal of utilizing stingless bees as alternative crop pollinators in Australia. VII Table of Contents AUTHOR ATTRIBUTION II PREFACE III STATEMENT OF AUTHORSHIP IV ACKNOWLEDGEMENTS V ABSTRACT VII CHAPTER 1: GENERAL INTRODUCTION 1 CHAPTER 2: Stingless bee floral visitation in the global tropics and subtropics 15 ABSTRACT 16 INTRODUCTION 17 METHOD 19 RESULTS 21 DISCUSSION 30 CONCLUSION 35 SUPPLEMENTARY INFORMATION 36 CHAPTER 3: Long-distance dispersal of males in the stingless bee Tetragonula carbonaria 51 ABSTRACT 52 INTRODUCTION 53 METHOD 55 RESULTS 62 DISCUSSION 69 CONCLUSION 72 SUPPLEMENTARY INFORMATION 73 CHAPTER 4: Irreversible sterility of workers and high-volume egg production by queens in the stingless bee Tetragonula carbonaria 87 ABSTRACT 88 INTRODUCTION 89 METHOD 90 RESULTS 93 DISCUSSION 98 CONCLUSION 100 SUPPLEMENTARY INFORMATION 101 VIII CHAPTER 5: Virgin queen behaviour and mating in the stingless bee Tetragonula carbonaria 109 ABSTRACT 110 INTRODUCTION 111 METHOD 113 RESULTS 118 DISCUSSION 127 CONCLUSION 130 SUPPLEMENTARY INFORMATION 131 CHAPTER 6: Reproductive communication and nest parasitism in an Australian social bee, Tetragonula carbonaria 134 ABSTRACT 135 INTRODUCTION 136 METHOD 138 RESULTS 144 DISCUSSION 152 CONCLUSION 156 SUPPLEMENTARY INFORMATION 157 CHAPTER 7: GENERAL DISCUSION 164 AUTHOR ADDRESSES 174 REFERENCES 175 IX CHAPTER 1 General Introduction 1. Bees as pollinators The importance of pollinators Pollination is one of the main ecosystem services provided to humanity (Klein et al., 2007, Kremen et al., 2002).
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