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A Multi-Level Analysis of the Interactions Between Vectors, Hosts, and Habitats of EEEV by Laura Kristin Estep a Dissertation S

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A Multi-Level Analysis of the Interactions Between Vectors, Hosts, and Habitats of EEEV by Laura Kristin Estep a Dissertation S A Multi-level Analysis of the Interactions between Vectors, Hosts, and Habitats of EEEV by Laura Kristin Estep A dissertation submitted to the Graduate Faculty of Auburn University in partial fulfillment of the requirements for the Degree of Doctor of Philosophy Auburn, Alabama May 9, 2011 Key words: dispersal kernel, forage ratio, arbovirus, mosquito, avian reservoir host, GIS Copyright 2011 by Laura Kristin Estep Approved by Geoffrey E. Hill, Chair, Professor of Biological Sciences Thomas R. Unnasch, Professor of Global Health, University of South Florida Bertram Zinner, Associate Professor of Mathematics and Statistics F. Stephen Dobson, Professor of Biological Sciences Arthur G. Appel, Professor of Entomology and Plant Pathology Abstract Eastern equine encephalitis virus (EEEV) is a rare and dangerous mosquito-borne pathogen with an elusive pattern of occurrence across its range in North America. The primary basis of our understanding of its transmission cycle between the vector Cs. melanura and avian reservoir hosts stems from studies in the northeastern United States. In this dissertation, I draw upon a range of innovative statistical approaches to study the transmission of EEEV in the southeastern United States in relation the ecology of EEEV vectors and avian reservoir hosts. I estimate the dispersal distance of Culex. erraticus, a mosquito species potentially involved in transmission of the virus, using a novel approach rooted in Bayesian statistics and borrowed from the seed dispersal literature. I also consider the distribution of avian reservoir hosts of the virus and their habitat associations, with the goal of estimating rates of utilization of avian host species by EEEV mosquito vectors. Such estimates of host utilization have great potential utility in revealing relative contribution of various hosts species to transmission of the virus. Indeed, I provide evidence that the most highly preferred host of Cs. melanura, the common yellowthroat (Geothylpis trichas), has the strongest support of influencing transmission as a dilution host among species considered. Finally, I develop model a to predict rates of contact of avian hosts with Cx. erraticus based on host characteristics using data on host traits available from the ornithological literature. Together these results of my studies provide a strong basis for the future development of predictive models for occurrence of the virus and provide a framework for ii future research of the transmission of this virus in the Southeast, and potentially throughout its range in North America. iii Acknowledgments This dissertation, from its inception to the final wording of its sentences, has been a collaborative effort. I thus have many people to thank for their guidance and support through this process. My graduate advisor and committee chair, Dr. Geoffrey Hill, constantly went above and beyond my expectations of a graduate advisor in terms of his encouragement, academic savoir-faire, and, in the critical periods of approaching deadlines, skillful editing. Above all else, I am grateful to him for teaching me to strive for and achieve clarity in my scientific thinking and writing. Dr. Thomas Unnasch provided me with a tremendous opportunity to focus my graduate studies by allowing me to collaborate on his research of eastern equine encephalitis virus. Without this opportunity I would not have been able to conduct the research I present in this dissertation. For this and his service on my committee, I am very grateful. I also am extremely grateful to Dr. F. Steve Dobson and Dr. Bertam Zinner for their willingness to collaborate on my graduate research as committee members, and Dr. Arthur Appel, for serving as an outside reader, as their collective service has ensured that this dissertation meets a high standard of quality for ecological and quantitative research. I also thank Dr. Hassan Hassan, Dr. Nathan Burkett-Cadena, Dr. Robert Unnasch, and PhD candidate Chris McClure, all of whom were involved in the data collection, analysis, and editing for one or more of these chapters. I would like to express my gratitude in particular to my student colleagues, Chris and Nathan, for demonstrating to me the essence of collaboration in scientific research during the preparation of this dissertation. I also thank Brian Rolek, Lisa McWilliams, iv Austin Mercadante, Katherine Gray, Chris Porterfield Nathan Click, and Dr. Christy Voakes for their roles in the field research and collection of data used for analyses in this research, and the labs of Dr. Hill and Dr. Wendy Hood for extensive editing of drafts of the chapters of this dissertation. Finally, I thank my family and loved ones, Diane, Kelly, and David Estep, and Brian Butler and Justin Hayes, for their steadfast support during my comprehensive examinations and the writing of this dissertation. v Table of Contents Abstract.........................................................................................................................................ii Acknowledgments........................................................................................................................iv List of Tables .............................................................................................................................viii List of Figures............................................................................................................................... x I. Estimation of dispersal distances of Culex erraticus in a focus of eastern equine encephalitis virus in the southeastern United States ............................................................................. 1 Abstract ........................................................................................................................... 1 Introduction ...................................................................................................................... 1 Materials and Methods ..................................................................................................... 4 Results ............................................................................................................................ 11 Discussion ...................................................................................................................... 13 References ...................................................................................................................... 17 II. A multi-year study of mosquito feeding patterns on avian hosts in a southeastern focus of eastern equine encephalitis virus .................................................................................... 28 Abstract ......................................................................................................................... 28 Introduction .................................................................................................................... 28 Materials and Methods ................................................................................................... 30 Results ............................................................................................................................ 36 Discussion ...................................................................................................................... 38 References ...................................................................................................................... 44 vi III. Developing models of avian host forage ratio models for Culiseta melanura and Culex erraticus using host characteristics................................................................................. 56 Abstract ......................................................................................................................... 56 Introduction .................................................................................................................... 56 Materials and Methods ................................................................................................... 59 Results ............................................................................................................................ 62 Discussion ...................................................................................................................... 64 References ...................................................................................................................... 69 IV. Using attributes of avian communities to predict local enzootic transmission of eastern equine encephalitis virus................................................................................................. 84 Abstract ......................................................................................................................... 84 Introduction .................................................................................................................... 84 Materials and Methods ................................................................................................... 88 Results ............................................................................................................................ 91 Discussion ...................................................................................................................... 93 References ...................................................................................................................... 95 vii List of Tables I. Table 1. Mean (95% credible intervals) for parameters and
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