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Effects of Bed Nets on Host Seeking Behaviour of African Malaria Vectors

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Effects of Bed Nets on Host Seeking Behaviour of African Malaria Vectors Effects of Bed Nets on Host Seeking Behaviour of African Malaria Vectors Thesis submitted in accordance with the requirements of the University of Liverpool for the degree of Doctor in Philosophy by Josephine Elizabeth Anne Parker November 2015 Abstract Long lasting insecticide treated bed nets (LLINs) are a key tool in malaria control in sub- Saharan Africa, and their widespread distribution has contributed significantly to recent reductions in malaria prevalence. Sustaining this impact will require thorough understanding of anopheline host seeking behaviour and LLIN mode of action. However, the behaviour of anopheline mosquitoes during interactions with LLINs, and how insecticides affect that behaviour, is poorly investigated. To pursue this, novel video systems, scaled to record and track nocturnally active free-flying mosquitoes at different levels of detail, were developed and evaluated in a series of behavioural studies, primarily with insecticide susceptible Anopheles gambiae s.s.. The spatial repellent properties of deltamethrin and DDT were investigated using two small-scale cage assays that presented mosquitoes with a human thumb bait and LLIN with (larger choice test) or without (smaller single test) an untreated control alternative. Results from single tests indicated repellency (in deltamethrin only) but the larger choice tests, (and subsequent large-scale tracking), did not. The results highlighted the limitations of such assays, and the caution required when otherwise convenient laboratory behavioural assays are used. The flight behaviour of host-seeking mosquitoes as they navigated through an open window was investigated in a laboratory environment using a novel 3D tracking system. The study proved the principle of this 3D tracking concept, which uses a retro-reflective material to identify a mosquito’s position during flight using a single camera. Analyses of tracks showed that mosquitoes approached windows from higher flight elevations, consistently descending to low levels following passage from the window into the room. Large scale tracking experiments used Fresnel lenses to illuminate a large field of view, and record activity of free flying An. gambiae s.s. at a human-baited bed net. These laboratory tests characterised mosquito flight into four behavioural modes, showing that insecticide treatment rapidly reduced mosquito activity around the net, and provoked a shift in flight behaviour resulting in less net contact. Highest levels of net contact were centred on the net roof above the volunteer’s torso. Insecticide treatment reduced the time a mosquito spent in contact with the net, and an individual mosquito was estimated to accumulate less than 100 seconds of direct physical contact with the LLIN during a 60-minute test. Velocity measurements showed that mosquitoes detected nets, including unbaited untreated nets, prior to contact. The large scale tracking system was transported to, and operated successfully at an experimental hut in Tanzania, to investigate the behaviour of a wild mosquito population consisting predominantly of An. arabiensis. Experimental outcomes were similar in both settings, though field tests did not show such pronounced activity decay as was observed in laboratory tests. The large-scale system was used to explore the host seeking flight behaviour of An. gambiae s.s. in the absence of a bed net. Flight activity at a supine human host was separated into approaching or departing tracks. Flight elevation and speed were similar in both, but tortuosity was higher in tracks approaching the host. Mosquitoes showed no preferences for feeding on any part of the host’s body and bites were distributed evenly across the volunteer’s exposed skin. This study delivers the most complete characterisations of mosquito-LLIN interactions to date. The tracking systems provide a new platform for a range of further studies and the findings contribute to evidence base required for vector control tool design, research on basic host seeking behaviour and the behavioural mechanisms of insecticide resistance. i Declaration This work has not been submitted previously for any other degree, and is not being currently submitted in candidature for another degree at this or any other university. The work presented in this thesis is the result of my own investigations. The contributions of the collaborating partners involved in the work are detailed below: All technological aspects of the insect tracking system, described in Chapter 2 and employed in Chapters 5-7, were designed and assembled by Dr Natalia Angarita- Jaimes, Dr Catherine Towers and Prof. David Towers. NAJ wrote the custom software used in Chapters 4-7, and undertook cleaning, tracking and post- processing of data used in Chapter 5. The illumination method used for tracking in Chapter 4 was conceived by DT and realised by NAJ. The “small scale assay A”, which was modified for use in the behavioural tests reported in Chapter 3, was designed by Mayumi Abe and Philip McCall. I was assisted in carrying out the experiments in Chapter 5 (MA and NAJ), 6 and 7 (NAJ). Signed: Date: 25th November 2015 Josephine Parker (Candidate) ii Acknowledgements The work described in this thesis could not have been completed without the support of many people. Philip McCall has been a constant source of guidance, and advice along the course of this PhD. His knowledge of the field and ambitious ideas have shaped this thesis, and I am grateful for his mentorship, and his infectious enthusiasm. When I signed up to this course I could not have anticipated how crucial a common interest in chocolate biscuits could be to a successful student-supervisor relationship. Natalia Angarita-Jaimes’ persistence and hard work in successfully completing the tracking software led her to spend many late nights at the computer, and continued well after she left the project. I am immensely grateful to her dedication to this work, for the generous application of her time, and for her willingness to come to the field (even when she didn’t have to). The beautiful tracking images and videos contained in this thesis could not have been produced without her creativity and perfectionism. I am grateful to Dave and Cathy Towers for their technical guidance and novel ideas which led to the new tracking methods developed for this work. This work would not have been possible without their help. Thanks also to Mayumi Abe who played an important role in the initial years of this project, and helped introduce me to mosquitoes and behavioural testing. This work could not have been completed without funding from Avecnet Consortium (financed by the European Commission’s Seventh Framework Programme).Thanks to my secondary supervisor Hilary Ranson for her leadership within this collaboration, and encouragement throughout my PhD. Thanks also to Eve Worrall, Sharon Mullane and Gillian Kyalo for their organisational roles ensuring the smooth running of many practical aspects of work in Liverpool and the field. During the course of field work I have received a great deal of support from NIMR Mwanza, thanks to the kind welcome of John Changalucha. Fabian Mashauri and Jackline Martine contributed a lot to the implementation of the tracking system in the field, and this work would not have been possible without their help. I’m grateful to Epifan and Sadatale for their work in maintenance of wild mosquito populations housed in the NIMR insectaries. I owe a debt of thanks to David Giesbrecht for his design and construction of the ‘flat-pack’ experimental hut. Benedict Wareba, Joseph Mbere, Sara Joseph and Herman Ukara played vital parts in the practical execution of field work. Their dedication to working strange hours iii conducting many unusual tasks helped ensure this project survived translation in to the field. Further thanks are extended to Charles for his beneficent permissions for work on his land, and for his liberal, persistent, but ultimately unsuccessful efforts to propose (via Herman). Back at the LSTM Kath Gleave deserves special thanks for her many hours of work software testing, tracking and processing data files. I could not have completed this work without her indefatigable persistence and excellent note taking. Brian Faragher contributed a great deal of guidance and statistical advice for the analysis methods used in this thesis. I am very grateful for his direction, and his enthusiasm for the artistic possibilities of our tracking images. Thanks also to Ghaith Aljayyoussi for his assistance with decay analyses. Maurane Riesen’s MSc project work on retro-reflective tracking helped in the interpretation and analysis of experiments in Chapter 4. Matt Hall’s undergraduate project provided many ideas which helped steer the final analysis of Chapter 7. I am very grateful to all volunteers who participated in tests. The generous contribution of their time, and willingness to endure hours lying still in a stuffy insectary/ experimental hut is much appreciated. Thanks to the LITE team for the provision of insects to start (and re-start) my mosquito colony, and for their help and advice in and out of the lab. This work has benefited from suggestions and ideas of past and present lab members Amy Guy, Ben Rogerson, Angela Hughes and Greg Murray. During field work I have been grateful to all my friends who read and replied to my long emailed newsletters. In Liverpool I’ve been supported along the way by the friendship of colleagues with long fun lunches in CTID. Particular thanks go to Joe Ryan, Jess McLachlan
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