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Population Biology and Landscape Ecology of Digenetic POPULATION BIOLOGY AND LANDSCAPE ECOLOGY OF DIGENETIC TREMATODE PARASITES IN THEIR GASTROPOD HOSTS, WITH SPECIAL EMPHASIS ON ECHINOSTOMA SPP. BY MICHAEL R. ZIMMERMANN A Dissertation Submitted to the Graduate Faculty of WAKE FOREST UNIVERSITY GRADUATE SCHOOL OF ARTS AND SCIENCE in Partial Fulfillment of the Requirements for the Degree of DOCTOR OF PHILOSOPHY Biology May 2014 Winston-Salem, North Carolina Approved By: Gerald W. Esch, Ph.D., Advisor Michael V. K. Sukhdeo, Ph.D., Chair Herman E. Eure, Ph.D. Erik C. Johnson, Ph.D. Miles Silman, Ph.D. Clifford W. Zeyl, Ph.D. ACKNOWLEDGEMENTS This dissertation could not have been completed without the help of a number of people along the way. First and foremost, this body of work would not have been the same without the collaboration and mentorship of Dr. Esch. His knowledge of parasitology, ecology, and sheer excitement for biology and discovering the unknown after nearly 50 years of mentorship were truly inspiring and helped shape me into the biologist, researcher, and person I am today. I will forever be grateful for his influence. I also would like to thank my committee members, Drs Eure, Johnson, Silman, Sukhdeo, and Zeyl for providing feedback, lab space , and endless banter that have greatly improved this dissertation. Additionally, I am also grateful to have spent my time at Wake Forest during both my Master’s degree and Ph.D. with fellow lab mate Kyle Luth. His input into data interpretation, statistical analyses, and writing has greatly improved my skills as a scientist. If you are going to spend 10 weeks in a van collecting snails, fishing, and camping with somebody, you better get along with them, and Kyle and I have become great friends as a result. I must also thank several of my other fellow graduate students. Daniel Griffith was integral in helping to formulate and design statistical analyses and the members of the Johnson lab helped keep my sanity while failing at molecular work through discussing moral conundrums such as the ethics of stealing bitcoins and seemingly daily debates of whether viruses are ‘alive’. Additionally, I would like to thank Mike Rizzo, who despite his efforts to contribute to research in the Each Lab, has never successfully hunted an animal or caught a fish in spite of 25+ years of effort. Despite this, he has remained a good friend and sport about being the butt of many jokes. ii There are also a few people to thank for inspiring my journey into biology and parasitology. First, I would like to thank my grandfather Joe Spenoso for influencing my foray into fishing and interest in aquatic life. Although I was unaware at the time, his guidance peaked my interest in all living things associated with aquatic environments and I would have not have taken the path I am on now without his influence. I also want to acknowledge my 7 th grade biology teacher, Marlene Osborn. It was after taking her class that I knew I wanted to pursue a career in biology. Her enthusiasm and initiative in creating a stimulating learning environment peaked my interest, a sentiment that never wavered. I would also like to thank my undergraduate mentor, Dr. Danny Ingold. His bolstered enthusiasm for teaching and life motivated me to pursue a graduate degree, which ultimately led to the completion of this dissertation. My family was also extremely supportive during my past 6 years at Wake Forest. My parents, sisters, and mother-in-law Liz have been extremely supportive in the pursuit of my graduate degrees. Pretending to be interested in my research (although not so much toward the end when they knew degree completion was imminent) and encouraging me along the way was much appreciated. Even though my Dad ‘would have been fired 3 and a half ye ars ago for taking this long to write a report’, the support from him and my Mom never faltered. Although I am the last of the Zimmermann children to earn their doctorate, I know my parents are proud and thank them for their encouragement and support. I would also like to thank my wife Abby, because without her this degree would not have been possible. She moved down to Winston-Salem when I started this degree, after spending two years apart when we were both completing our Master’s degree, iii probably the longest two years of my life. Her support and urging (although it was probably more like shoving at times) allowed me to complete this degree. Additionally, her taking care of the duties at home despite working a full-time job were much appreciated, even though I will probably have to wash the dishes for the next year. Thank you again Abby for your love and support. Finally, I would like to dedicate this dissertation to Grandma Esther. Although she passed away in the early stages of this degree, just prior to her 97 th birthday, nobody would have been more excited to see me complete this dissertation. Despite her having to overcome the fact that I am a Republican, she let me be her cribbage partner and always treated me as if I was her own grandchild. Her joy and zest for life, in the face of dealing with bouts of macular degeneration, were truly an inspiration and have made me a better person. I promise that someday she will finally get her rematch with my parents in that game of euchre. iv TABLE OF CONTENTS Page ACKNOWLEDGEMENTS……………………………………………………………… ii LIST OF TABLES.. …………………………………………………………………… ....ix LIST OF FIGURES.. ……………………………………………………………………. .xi ABSTRACT…………………………………………………………………………… .xvi CHAPTER I Introduction and study sites BACKGROUND.. ………………………………………………………...1 STUDY SITES MALL ARD LAKE……………………………………………......9 COON LAKE…………………………………………………….12 OTHER U. S. SAMPLE SITES………………………………… ..14 LITERAT URE CITED…………………………………………………..15 CHAPTER II Digenetic trematode life cycles shape their infection patterns in their pulmonate snail hosts ABST RACT……………………………………………………………..47 INTR ODUCTION……………………………………………………….48 MATERIALS AND METHODS………………………………………...51 RESULTS………………………………………………………………..54 DIS CUSSION……………………………………………………………58 LITERATU RE CITED………………………………………………….. 69 v CHAPTER III Infection pattern differences of digenetic trematode parasites across the North American waterfowl flyways ABSTRACT ……………………………………………………………..99 INTRODUCTION ……………………………………………………...100 MATERIALS AND METHODS ……………………………………….103 RESULTS ………………………………………………………………104 DISCUSSION …………………………………………………………..105 LITERATURE CITED ………………………………………………… 110 CHAPTER IV Habitat disturbance affects the distribution of trematode parasites among a pulmonate snail community ABST RACT…………………………………………………………….134 INTR ODUCTION………………………………………………...……135 MATERIALS AND METHODS……………………………………….137 RESUL TS……………………………………………………………....1 39 DISCUS SION…………………………………………………………..141 LITERATURE CITED………………………………………………… 145 Submitted to the Journal of Limnology (In Review) CHAPTER V Differences in microhabitat affect parasite transmission in Helisoma anceps ABS TRACT…………………………………………………………….156 INTROD UCTION……………………………………………………...157 vi MATERIAL S AND METHODS……………………………………….160 RE SULTS………………………………………………………………163 DISCUSSION…………………………………………………………..165 LITERA TURE CITED…………………………………………………169 Submitted to Freshwater Science (In Review) CHAPTER VI Transmission pattern differences of miracidia and cerceriae larval stages of digenetic trematodes in relation to snail size and density ABS TRACT…………………………………………………………….178 INTROD UCTION……………………………………………………...179 MATERIAL S AND METHODS……………………………………….182 RE SULTS………………………………………………………………184 DISCU SSION…………………………………………………………..186 LITERA TURE CITED…………………………………………………1 91 Submitted to the Comparative Parasitology (In Review) CHAPTER VII Auto-infection by Echinostoma spp. in nature ABSTRACT ………………………………………………………….....204 INTROD UCTION……………………………………………………...205 MATERIAL S AND METHODS……………………………………….208 RE SULTS………………………………………………………………210 DISCUSSION…………………………………………………………..213 LITERA TURE CITED…………………………………………………218 vii CHAPTER VIII Differential infection patterns of Echinostoma spp. in snails belonging to three different families ABS TRACT…………………………………………………………….230 INTROD UCTION……………………………………………………...231 MATERIALS AND METHODS………………………………………. 235 RESUL TS……………………………………………………………....237 DISCUSSION………………………………………………………… ..240 LITERATURE CITED………………………………………………… 246 Submitted to Acta Parasitologica (In Press) CHAPTER IX The dilution effect in Echinostoma spp.: Examples from field collected data ABS TRACT…………………………………………………………….257 INTROD UCTION……………………………………………………...2 58 MATERIALS AND METHODS……………………………………….262 RE SULTS………………………………………………………………264 DISCUSSION…………………………………………………………..266 LITERA TURE CITED…………………………………………………273 CHAPTER X Summary ………………………………………………………………………..290 APPENDIX …………………………………………………………………………… ..298 CURRICULUM VITAE……………………………………………………………….. 341 viii LIST OF TABLES Table I-1. Fish, amphibian, and reptile species observed in Mallard Lake ……………..22 Table I-2. Bird species observed visiti ng Mallard Lake………………………………...23 Table I-3. Parasite species, the hosts from which they were recovered, and the parasitic stage recovered from Mallard Lake ……………………………..……...24 Table I-4. Vertebrate species observed in Coon Lake in the summer of 2013 ………….25 Table I-5. Parasite species, the hosts from which they were recovered, and the parasitic stage recovered from Coon Lake ………………………………………………...26 Table I-6. Snail species and the number collected from sample sites across t he U.S.….27 Table II-1. Trematode parasite species found in Mallard Lake…..……………………..77 Table II-2. Trematode parasites infecting H. anceps in Charlie’s Pond………………...78 Table II-3. Trematode
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