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Improving the Handling, Transport and Release of Sterile Male Mosquitoes As Part of an Area-Wide Integrated Pest Management Strategy

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Improving the Handling, Transport and Release of Sterile Male Mosquitoes As Part of an Area-Wide Integrated Pest Management Strategy Improving the Handling, Transport and Release of Sterile Male Mosquitoes as Part of an Area-wide Integrated Pest Management Strategy Thesis submitted in accordance with the requirements of the University of Liverpool for the degree of Doctor of Philosophy Nicole Jean Culbert April 2020 ___________________________________________________ Abstract Improving the Handling, Transport and Release of Sterile Male Mosquitoes as Part of an Area-wide Integrated Pest Management Strategy By Nicole Jean Culbert The global burden of vector-borne diseases continues to grow year on year. Diseases transmitted by mosquitoes lead to more than 700,000 deaths each year, with malaria alone accounting for almost half a million of the total deaths. Such statistics underline the urgency for alternative complementary control measures. The sterile insect technique (SIT) is one of several genetic control measures routinely used throughout the world to suppress, contain or eradicate various species of agricultural, veterinary or human insect pests. SIT is a technique which has proved successful and sustainable, particularly when deployed as part of an area-wide integrated pest management programme (AW-IPM). A build-up of insecticide resistance coupled with the global spread of species such as Aedes aegypti and Aedes albopictus has reignited interest in developing mosquito SIT as part of an AW-IPM approach. Significant progress has been made in the last decade towards taking mosquito SIT to the operational level, however, distinct gaps still remain in the literature, especially regarding the post-pupal irradiation stages. The aim of this research thesis was to address some of the key issues where information was lacking, specifically the handling, transport and release of sterile male mosquitoes. The impact of immobilisation temperature and duration on male mosquito survival was investigated in Aedes aegypti, Aedes albopictus and Anopheles arabiensis, in order to determine a suitable storage and transportation temperature range when conducting releases of sterile male mosquitoes. The effect of compaction during storage was investigated and a maximum tolerable threshold determined. A standardised method to mark male mosquitoes for a small-scale field release was developed and verified in Aedes aegypti, Aedes albopictus and Anopheles arabiensis. A novel flight ability device, which aims to assess male mosquito quality was created and validated for Aedes aegypti, Aedes albopictus and subsequently modified and verified for Anopheles arabiensis.The effect of varying environmental conditions relating to the time of day that sterile male releases could occur was investigated for both male Anopheles arabiensis and Aedes aegypti. Finally, an adult aerial release device was developed in conjunction with the NGO WeRobotics and as part of a United States Agency for International Development grant. The system was successfully field tested in Brazil via a series of mark-release-recapture studies. As mosquito SIT nears the operational phase, it is hoped this research is a starting point when addressing some of the outstanding questions related to the handling, transport and release of sterile male mosquitoes. ii _____________________________________________ Declaration I declare that this thesis has not been previously submitted for any other degree or professional qualification. This thesis is the result of my own investigations. The results presented in chapters 2 – 8 were obtained in collaboration with others, whose contributions were as follows: Chapter 2: Conceptualisation and experimental design: NJCa and JRLGb. Experimental work: NJC. Data interpretation and analysis: NJC. Supervision: JRLG and RSLc. Writing original draft: NJC. Writing – review and editing: NJC, RSL, MJBVd, ACDe and JRLG. Chapter 3: Conceptualisation and experimental design: NJC and JRLG. Experimental work: NJC. Data interpretation and analysis: NJC and JB. Supervision: JRLG. Writing original draft: NJC. Writing – review and editing: NJC, JRLG and JBf. Chapter 4: Conceptualisation and experimental design: NJC, FBg, ADh, GSHi and JB. Experimental work: NJC, TWj and HYk. Data interpretation and analysis: NJC and JB. Supervision: JB. Writing original draft: NJC. Writing – review and editing: NJC, FB, AD, GSH, HY, TW and JB. Chapter 5: Conceptualisation and experimental design: NJC and JB. Experimental work: NJC, NSBSl, DDSm, SCn, TW, HMo and WMp. Data interpretation and analysis: NJC and JB. Supervision: JB. Writing original draft: NJC. Writing – review and editing: NJC, NSBS, DDS, SC, TW, HM, WM, HY and JB. iii Chapter 6: Conceptualisation and experimental design: NJC, MKq, NVr and JRLG. Experimental work: NJC, MK and NV. Data interpretation and analysis: NJC and JB. Supervision: JRLG and JB. Writing original draft: NJC. Writing – review and editing: NJC, MK, NV, MJBV, JRLG and JB. Chapter 7: Conceptualisation and experimental design: NJC, JRLG and WM. Experimental work: NJC, HM, NSBS and WM. Data interpretation and analysis: WM. Supervision: JRLG. Writing original draft: NJC and WM. Writing – review and editing: NJC, HM, NSBS, JRLG, JB and WM. Chapter 8: Conceptualisation and experimental design: JB, NJC, JVs and RAHt. Experimental work: NJC, MGu, AKv, JGw, TW, GSH, RAH, HY and FB. Data interpretation and analysis: AHDx and JB. Supervision: JB and JV. Writing original draft: JB, NJC, AHD, MG, JG and RAH. Writing – review and editing: JB, NJC, AHD, MG, JV, AK, JG, TW, GSH, RAH, HY, FB and MJBV. aNicole J. Culbert; bJeremie R. L. Gilles; cRosemary S. Lees; dMarc J. B. Vreysen; eAlistair C. Darby; fJérémy Bouyer; gFabrizio Balestrino; hAriane Dor; iGustavo S. Herranz; jThomas Wallner; kHanano Yamada; lNanwintoum S. B. Somda; mDieudonné D. Soma; nSilvana Caravantes; oHamidou Maiga; pWadaka Mamai; qMaria Kaiser; rNelius Venter; sJair Virgilio; tRafa A. Herrero; uMaylen Gomez; vAdam Klaptocz; wJurg Germann; xAhmidou H. Dicko. Signed ……………………………………………………………………. (candidate) Date ………………………………………………………………………. iv _____________________________________________ Acknowledgements First and foremost, I would like to express the utmost gratitude to my supervisors, Dr Jérémy Bouyer and Dr Alistair Darby, for their endless support, guidance, encouragement and tuition during both the research and writing elements of this thesis. I further extend my thanks to my previous group leader Dr Jeremie Gilles with whom I began this journey and who actively encouraged me to pursue this PhD. To all past and present members of the Insect Pest Control Laboratory, I thank you for your boundless advice and support during my research. To my work besties, Hanano and Thomas (clap clap), you kept me sane during some tough times and always managed to put a smile on my face when it was most needed, vielen Dank! I would like to thank my Mum and brother for their unwavering support throughout the thesis, despite the curveball life threw at us in the midst of it all. To all the friends I made along the way during my years in Vienna and to all my friends scattered across the globe, thanks for letting me bore you with my mosquito-related geek facts or for offering a shoulder of support when needed. To my boyfriend and best friend, thanks for seeing me through the end of this journey, encouraging me as a scientist ever since those Deen days and for teaching me to follow my dreams. I love you. The biggest thank you of all has to go to my best friend forever, my soul sister and my partner in crime, Silvana. If anyone got me through these past few years it was you. You have always been by my side when I needed you and if you weren’t, you were just a Facebook video call away. Thanks for always believing in me. From staying late v in the lab helping me with my mozzies, to bringing me a McDonalds coffee every morning. Thank you for every last thing you did for me. Finally, I would like to acknowledge the selfless support of all of the collaborators in each of the chapters of this thesis. Thank you all. vi _____________________________________________ Dedication I started this journey with you by my side and yet I must finish it alone. This one’s for you Dad. vii _____________________________________________ Table of Contents Abstract ……………………………………………………...…….…… ii Declaration …………………………………………………...……….. iii Acknowledgements …………………………………………….…….… v Dedication ………………………………………………………...…... vii Table of Contents …………………………………………………...…viii List of Figures ………………………………………………………... xiii List of Tables …………………………………………...………..….. xvii Abbreviations ……………………………………...…………………. xxi Chapter 1: Introduction ……………….……………………………… 1 1.1 The World’s Deadliest Animal ……………………..…………………………… 2 1.2 A Global Concern ………………………………………………..……………… 4 1.3 Alternative Vector Control Solutions ……………………………………..…….. 5 1.4 The Birth of the Sterile Insect Technique ………………………………...……... 9 1.5 Sterile Insect Technique Successes Against Other Diptera ………………….…. 11 1.6 Sterile Insect Technique Successes Against Lepidoptera ……………......…….. 13 1.7 Historical Applications of the Sterile Insect Technique Against Mosquitoes ….. 16 1.8 Recent Applications of the Sterile Insect Technique Against Mosquitoes …..... 17 1.9 Developing the Mass Rearing Process for Sterile Insects: Pre-irradiation ……... 20 1.9.1 Larval Rearing ………….…………………………..………...………….… 20 1.9.2 Larval Diet …………...………………………………………...………...… 22 1.9.3 Sex Separation …….……..…………………………………...……………. 23 1.9.4 Irradiation …………..…...….……………………………………………… 26 1.9.5 Mass Rearing Cages …………..………...……………….……………….... 28 1.10 Mass Rearing
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