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Vectorial Capacity Across an Environmental VECTORIAL CAPACITY ACROSS AN ENVIRONMENTAL GRADIENT NICHAR GREGORY Department of Life Sciences Imperial College London A thesis submitted for the degree of Doctor of Philosophy 2019 1 “Mosquitoes are certainly our declared enemies, and very annoying enemies at that. But they are enemies good for us to know. If we give them even the least bit of attention we find ourselves forced to admire them and to admire even the instrument they bleed us with; for this it is only necessary to examine their structure. Furthermore, throughout their lives they offer facts adequate to please any of those minds which are curious about the marvels of nature. There are even times in the mosquitoes’ lives when, having made the observer forget that they’ll persecute him some day, they make him feel actually, solicitous about their welfare” - De Rèaumur’s (1740) 2 Declaration of Originality I declare that the work described in this thesis is my own, except where stated, and that I have compiled it in my own words. Where others are included as authors on individual chapters, those individuals have provided comments on that chapter. Two anonymous reviewers provided a great deal of insight into the analyses in Chapter 3 when that chapter was submitted for publication in Environmental Research Letters. Copyright declaration The copyright of this thesis rests with the author. Unless otherwise indicated, its contents are licensed under a Creative Commons Attribution-Non Commercial 4.0 International Licence (CC BY-NC). Under this licence, you may copy and redistribute the material in any medium or format. You may also create and distribute modified versions of the work. This is on the condition that: you credit the author and do not use it, or any derivative works, for a commercial purpose. When reusing or sharing this work, ensure you make the licence terms clear to others by naming the licence and linking to the licence text. Where a work has been adapted, you should indicate that the work has been changed and describe those changes. Please seek permission from the copyright holder for uses of this work that are not included in this licence or permitted under UK Copyright Law. 3 ABSTRACT Disease transmitted by mosquitoes present some of the most pressing challenges facing human health today. Land-use change is a key driver of disease emergence, however the mechanisms linking environmental covariates of change, such as temperature, to the transmission potential of mosquitoes is poorly understood. Studies exploring these relationships have largely been correlative in nature, and thus have limited capacity to predict dynamics through space and time. Mechanistic approaches provide a valuable framework for understanding the processes underlying transmission, however they suffer from a dearth of field data on fundamental mosquito ecology. In both approaches, the environmental data used is typically coarse in scale and interpolated from weather stations located in open areas. In reality, local climatic conditions can vary considerably over fine spatial and temporal scales, particularly in dynamic working landscapes. Wild mosquitoes experience and respond to this highly dynamic environment, and failing to account for this variation may have significant implications for the accuracy of epidemiological models. This thesis uses an established epidemiological framework to explore the effects of tropical forest conversion to oil palm plantation on the potential for Ae. albopictus mosquitoes to transmit disease. Using field-derived microclimate data and published thermal responses of mosquito traits, I first examine how the scale of environmental data affects predictions of mosquito demography under land-use change. Next, I conduct field experiments to investigate whether microclimate heterogeneity across a land-use gradient drives variation in the rates of larval development. By pairing fine-scale microclimate data with temperature- dependent trait estimates, I find that forest conversion significantly increases the potential of Ae. albopictus to transmit disease. Together, these findings advance our understanding of Ae. albopictus ecology, and highlight the importance of incorporating fine-scale environmental and mosquito data into epidemiological frameworks to better understand disease risk in changing landscapes. 4 Table of Contents List of Tables & Figures ............................................................................................................... 7 Acknowledgments ......................................................................................................................... 8 CHAPTER 1 : BACKGROUND ..................................................................................................... 10 1.1 The emergence of mosquito-borne diseases .................................................................... 10 1.2 Mosquito ecology: the linchpin of effective disease control ........................................... 14 1.3 Predicting disease transmission in dynamic environments .......................................... 20 1.4 Tropical forest conversion, oil palm plantations and vectorial capacity ....................... 22 1.5 Aedes-transmitted arboviruses in Malaysia ................................................................... 26 1.6 The Asian tiger mosquito (Aedes albopictus) ................................................................ 27 CHAPTER 2: Aims and objectives ........................................................................................... 28 2.1 Research aims and objectives ......................................................................................... 28 2.2 Thesis outline ................................................................................................................. 29 2.3 Study area ....................................................................................................................... 32 CHAPTER 3: Methodology ......................................................................................................... 36 3. 1 Data sources ................................................................................................................... 36 3.1.1 Temperature ................................................................................................................................................ 36 3.1.2 Thermal trait responses ........................................................................................................................ 37 3. 2 Estimating mosquito population growth rates (rmax) ................................................... 38 3.3 Field data ......................................................................................................................... 41 3.3.1 Larval experiments .................................................................................................................................. 41 3.3.2 Human landing catches ........................................................................................................................ 42 3.4 Derived parameters ........................................................................................................ 43 3.4.1 Estimating adult mosquito survival ................................................................................................ 43 3.4.2 Vectorial capacity ..................................................................................................................................... 45 3.5 Statistical analysis .......................................................................................................... 46 3.6 Ethical statement ......................................................................................................................................... 49 CHAPTER 4: DISTURBANCE-MEDIATED MICROCLIMATE DETERMINES INTRINSIC POPULATION GROWTH OF MOSQUITOES .................................................................................. 50 4.1 ABSTRACT ...................................................................................................................... 50 4.2 Introduction .................................................................................................................... 51 4.3 Results ............................................................................................................................ 55 4.3.1 Effects of drought and land-use on diurnal temperature cycles ...................................... 55 4.3.2 Effects of land-use and drought on predicted performance of Ae. albopictus traits ............................................................................................................................................................................................... 57 4.3.3 Temperature-sensitive rmax ................................................................................................................. 62 4.4 Discussion ....................................................................................................................... 64 CHAPTER 5 ..................................................................................................................................... 71 EL NIÑO DROUGHT AND TROPICAL FOREST CONVERSION SYNERGISTICALLY DETERMINE MOSQUITO DEVELOPMENT RATE ........................................................................ 71 5.1 ABSTRACT ....................................................................................................................... 71 5.2
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