ECOLOGICAL DYNAMICS OF VECTOR-BORNE DISEASES IN CHANGING ENVIRONMENTS by Luis Fernando Chaves A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy (Ecology and Evolutionary Biology) in The University of Michigan 2008 Doctoral Committee: Professor Mark L. Wilson, Co-Chair Associate Professor Mercedes Pascual, Co-Chair Professor John H. Vandermeer Assistant Professor Edward L. Ionides “Se puderes olhar, vê. Se podes ver, repara” Jose Saramago © Luis Fernando Chaves All rights reserved 2008 To my grandfather (Don Fernando), with love for his support and advice ii ACKNOWLEGEMENTS I am indebted to many people, primarily to my committee, they helped me in directing and defining my research agenda for this dissertation. First I’d like to thank my two chairs, Dr. Mercedes Pascual and Dr. Mark Wilson. They are very different in almost everything you can imagine, with the exception of being excellent scientists. With one I’m very grateful for the financial support, technical advice and input on scientific questions. With the other I’m grateful for the inspiration to build a comprehensive and dialectic epistemological framework for my career, and for the constant support through several steps in this segment of my journey in Academia. Dr. Ed Ionides was very helpful through his classes and time to instruct me with tools that are fundamental to the analysis of the problems presented here, as well as with the insights and perspectives of somebody with a completely different training. Dr. John Vandermeer is definitively one of my most admired colleagues, he showed me that being a successful ecologist can only be enhanced by being actively involved in the context of our objects/subjects of study. I am also very grateful to all the comrades from the three discussion groups I regularly attended during my stay at the University of Michigan: Plant Animal interactions (Rathcke and Hunter Labs), Tropical Biology (Perfecto, Dick and Vandermeer labs) and New World Agriculture and Ecology Group (too many iii people to mention). These groups widened my perspectives on the science of Ecology and led me to an intense collaboration with Sandra Yap, Rachel Vanette, Brian Sedio, Javier Ruiz and Shalene Jha, to whom I’m deeply grateful for all what they taught me about their research and for inviting me to apply my knowledge in areas outside where it is usually applied. Besides, all of them are among the best friends somebody could wish. Casey Taylor, Sandra Yap and Brian Sedio were also very generous with their time carefully reading and editing some of my manuscripts. I am also grateful to my labmates from the Pascual and Wilson labs, especially Justin Cohen for sharing ideas on spatial analysis and his input on epidemiological methods, and his generous help leading to the publication of Chapter VI. I am also grateful to all those friends with whom I kept contact and constantly gave me input on my research: Chepina Hernandez and Diego Rodriguez at Universidad Central de Venezuela; Tomas Revilla at Groningen University, Sander Koenraadt at Wageningen University, Menno Bouma at London School of Tropical Medicine and Hygiene, Andy Dobson at Princeton University and Dick Levins at Harvard School of Public Health. Christian Lengeler and Tom Smith helped me with their expertise on malaria bednets (chapters IV & V) during a visit to the Swiss Tropical Institute. Akira Kaneko and Anders Björkman gave significant input to chapters IV and V, and generously invited me iv to give a series of Lectures in their Malaria course at Karolinska Institutet in Stockholm during fall 2007, and to eventually join their group. Finally, I want to thank all the good friends I met in Ann Arbor: Liz Vivas, Jose Manuel Gomez, Jasun Gong, Courtney Murdock, David Alonso, Katie Pethan, Jerry Smith, Catherine Badgley, Robyn Burham, Dan Green, Alan Stapledon, Stefano Allesina, Lia Florey, Liz Lehman, Pete Boldenow, Jose Siri, Jahi Chappell, Kacey Ernst, Ting-Wu Chuang, Ben-Yang Liao, Dave Nicoletti Allen, Michael H. Reiskind, Anne Lippert, Doug Jackson, Julie Maslovsky, Eladio Marquez, Roosevelt Garcia, C. I. Flores, Diego Fernando Alvarado, Susana Pereira, Kat Connors and Natalie Hubbard. They made joyful and pleasant the time in Ann Arbor. v TABLE OF CONTENTS DEDICATION. ....................................................................................................... ii ACKNOWLEDGEMENTS .................................................................................... iii LIST OF TABLES ................................................................................................ ix LIST OF FIGURES ............................................................................................... x LIST OF APPENDICES ...................................................................................... xii ABSTRACT ........................................................................................................ xiii CHAPTER I INTRODUCTION ECOLOGICAL NATURE OF HUMAN DISEASES ...................................... 1 MALARIA AND AMERICAN CUTANEOUS LEISHMANIASIS ...................... 5 RESEARCH AGENDA ....................................................................... 7 REFERENCES .............................................................................. 11 CHAPTER II CLIMATE CHANGE AND THE ABILITY TO FORECAST DISEASES: I. NON-STATIONARY PATTERNS FOR AMERICAN CUTANEOUS LEISHMANIASIS IN COSTA RICA INTRODUCTION ............................................................................ 15 METHODS .................................................................................... 17 RESULTS ..................................................................................... 20 DISCUSSION ................................................................................ 22 REFERENCES .............................................................................. 34 CHAPTER III CLIMATE CHANGE AND THE ABILITY TO FORECAST DISEASES: II. NON-LINEAR TOOLS APPLIED TO AMERICAN CUTANEOUS LEISHMANIASIS FORECASTS IN COSTA RICA INTRODUCTION ............................................................................ 38 METHODS .................................................................................... 40 RESULTS ..................................................................................... 43 vi DISCUSSION ................................................................................ 44 REFERENCES .............................................................................. 54 CHAPTER IV MODELLING DISEASES FROM FIRST PRINCIPLES: SELF REGULATORY FEEDBACKS, BIOLOGICAL INTERACTIONS AND CLIMATIC FORCING, THE ECOLOGICAL DYNAMICS OF VIVAX AND FALCIPARUM MALARIA INTRODUCTION ............................................................................ 59 METHODS .................................................................................... 62 RESULTS ..................................................................................... 70 DISCUSSION ................................................................................ 71 REFERENCES .............................................................................. 82 CHAPTER V RESILIENCE TO THE EFFECTS OF ENVIRONMENTAL VARIABILITY: BEDNETS AND MALARIA IN VANUATU INTRODUCTION ............................................................................ 90 METHODS .................................................................................... 92 RESULTS ..................................................................................... 98 DISCUSSION .............................................................................. 101 REFERENCES ............................................................................ 119 CHAPTER VI THE ECOLOGICAL DYNAMICS OF VECTOR-BORNE DISEASES UNDER THE EFFECTS OF A MULTIDIMENSIONAL CHANGING ENVIRONMENT: SPATIAL PATTERNS OF CUTANEOUS LEISHMANIASIS; THE ROLE OF SOCIAL MARGINALITY AND DEFORESTATION IN COSTA RICA INTRODUCTION .......................................................................... 127 METHODS .................................................................................. 129 RESULTS ................................................................................... 135 DISCUSSION .............................................................................. 138 REFERENCES ............................................................................ 157 vii CHAPTER VII CONCLUSIONS SUMMARY OF MAJOR FINDINGS AND RESEARCH IMPLICATIONS ........ 162 SUGGESTIONS FOR FUTURE RESEARCH ........................................ 163 REFERENCES ............................................................................ 165 APPENDICES………….. .................................................................................. 167 viii LIST OF TABLES Table 2.1. Model Selection and Parameter Values ............................................ 25 Table 3.1. Models and predictive R2 .................................................................. 50 Table 4.1. Model Search. ................................................................................... 76 Table 4.2. Parameter estimates for the best models .......................................... 77 Table 5.1. Parameter values and % reduction for Plasmodium falciparum and Plasmodium vivax rate before and after the breakpoint obtained by using the variance of the Kolmogorov-Zurbenko adaptive filter. ...................................... 109 Table 6.1. Breakpoint