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The Role of Arthropod Second Intermediate Hosts As Avenues for and Constraints on the Transmission of Frog Lung Flukes (Digenea

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The Role of Arthropod Second Intermediate Hosts As Avenues for and Constraints on the Transmission of Frog Lung Flukes (Digenea THE ROLE OF ARTHROPOD SECOND INTERMEDIATE HOSTS AS AVENUES FOR AND CONSTRAINTS ON THE TRANSMISSION OF FROG LUNG FLUKES (DIGENEA: HAEMATOLOECHIDAE) By Matthew G. Bolek A DISSERTATION Presented to the Faculty of The Graduate College at the University of Nebraska In Partial Fulfillment of Requirements For the Degree of Doctor of Philosophy Major: Biological Sciences Under the Supervision of Professor John Janovy Jr. Lincoln, Nebraska May, 2006 THE ROLE OF ARTHROPOD SECOND INTERMEDIATE HOSTS AS AVENUES FOR AND CONSTRAINTS ON THE TRANSMISSION OF FROG LUNG FLUKES (DIGENEA: HAEMATOLOECHIDAE) Matthew G. Bolek, Ph.D. University of Nebraska, 2006 Advisor: John Janovy Jr. Avenues for and constraints on the transmission of frog lung flukes to frog definitive hosts were studied through examination of the role and fate of parasite metacercariae stages. This study was based on four species of North American frog lung flukes, Haematoloechus coloradensis (Cort, 1915), H. complexus (Seely, 1906), H. longiplexus Stafford, 1902 and H. parviplexus Stafford, 1902. Semi-terrestrial leopard frogs are commonly infected with Haematoloechus coloradensis and H. complexus but exhibit ecological host specificity and are rarely infected with H. parviplexus and H. longiplexus. The latter two lung flukes infect aquatic bullfrogs. Field and experimental infection data indicated that leopard frogs became infected with H. coloradensis and H. complexus by feeding on small non-odonate arthropods that served as second intermediate hosts for these parasites. Comparative experimental examinations of metacercarial survival patterns and distribution in second intermediate odonate hosts revealed that most metacercariae of H. longiplexus were lost during dragonfly metamorphosis, but most metacercariae of H. coloradensis, H. complexus, and H. parviplexus survived dragonfly metamorphosis. These observations suggest that the ecological host specificity of H. longiplexus in semi-terrestrial leopard frogs is due to few metacercariae of H. longiplexus reaching these frogs in a terrestrial environment. Experimental infections of leopard frogs and bullfrogs with H. parviplexus indicate that leopard frogs are resistant to infection with this species. This result indicates that the synonymy of worms from leopard frogs and bullfrogs is not warranted and species from leopard frogs and bullfrogs are distinct. A phylogenetic study of 12 species of North American and European frog lung flukes was conducted using the internal transcribed spacer region. The phylogenetic analysis revealed that these different lineages shared similar patterns of arthropod host specificity distinct from patterns found in the other lineages. These results suggest that second intermediate host specificity may be a trait that has been conserved through evolutionary time. The phylogenetic data presented in this study reveal the importance of second intermediate host specificity among the evolutionary lineages of frog lung flukes because second intermediate hosts serve as avenues for and constraints on the movement of these parasites to their respective definitive amphibian hosts. i ACKNOWLEDGMENTS Foremost, I would like to thank to my major professor, Dr. John Janovy Jr., for his guidance and friendship throughout this project and his acceptance of my many other side projects. He allowed me the absolute freedom to conduct studies on numerous amphibian parasite life cycles even though at times these studies must have seemed chaotic. I will always be grateful for his patience and support. Secondly, I would like to thank him for giving me the opportunity and constant guidance in preparing lectures for Invertebrate Zoology, Parasitology, Bios 101, and Introductory Zoology while teaching lectures at UNL. John is truly one of a kind teacher that always has a significant and effective lesson plan in mind for students. Finally, I credit Dr. Janovy as having not only shaped me as a biologist and a teacher but as a human being and a professional. I received my best learning experiences from him in the classroom, the field, and the Coffee House. I also thank the other members of my committee: Drs. Brent B. Nickol, George E. Veomett, Gwen Bachman, and William E. Wagner. All of these individuals have influenced my career as a graduate student and added greatly to my studies and research project. I greatly acknowledge Dr. Scott Snyder, University of Nebraska at Omaha for all of his help with the molecular aspect of this study. Scott welcomed me into his lab and allowed me the use of all of his equipment and his time to complete the molecular part of this work. He also freely shared all of his knowledge and his specimen collection of frog lung flukes that made this study possible. His help is greatly appreciated and his enthusiasm for the use of molecular tools to study trematode evolution was contagious. ii Many thanks are due to the faculty and staff of Cedar Point Biological Station and the many land owners of Nebraska who readily gave their permission to collect frogs, arthropods, and snails. CPBS is an outstanding place to teach and conduct biological research. Dr. Rich Alward, Rob Anderson, and Roy and Kathy Bailey were always willing to help and provide me with resources and space I needed to conduct my field and laboratory work. Completion of a Doctoral dissertation in parasitology is an endeavor which begins long before entrance into a Ph.D. program. My interests in parasitology and amphibian biology were fostered during my undergraduate career at Carroll College. I thank my undergraduate mentors Drs. John Mellen and Leslie Zettergren for introducing me to these critters and taking the time to discuss numerous projects on their biology. I was fortunate during my graduate education to learn from the best in the business including Dr. James R. Coggins, my masters advisor at the University of Wisconsin-Milwaukee, Drs. Kevin R. Kazacos and John MacDonald at Purdue University, and most importantly Drs. John Janovy Jr. and Brent Nickol at UNL. These individuals have taught me the professionalism and passion for parasitology. I thank the many graduate students whose input and help over the last few years were invaluable to the completion of this study and my understanding of scientific investigations. During my first few years, Ben Hanelt, Jaclyn Helt, AKA the secretary, Jill Detwiler, Samana Schwank, Michelle Steinauer, and Sara Brant helped me get started. The peer group, with whom I shared the last portion of my Ph.D. study, include Alaine Knipes, Gabriel Langford, Laura Duclose, Terry Haverkost, and Dave Tinnin. These individuals have influenced and refined my thought processes on parasite life cycle iii evolution and have helped me physically and mentally over the years. They have served as field assistants, consultants, editors, and most importantly my friends. Dr. Agustín Jiménez-Ruiz is a close friend who made my life in Lincoln an outstanding experience. Our discussions about parasitology and science have always been provocative and stimulating. His input as a reviewer on numerous manuscripts, and kind suggestions about research and the business of parasitology, are greatly appreciated. I would like to acknowledge my parents, Margaret and George Bolek, and my brother Luke Bolek for their support and understanding during my years in school. Without their support this work would have been impossible. Finally, I would like to thank my wife, Melissa Bolek, for her continuous moral support, understanding and sacrifices. She has been my most ardent supporter and was always there for me during the bad and good times. Mel was a great field assistant on those cold rainy nights in Wisconsin and Indiana and hot dusty nights in Western Nebraska. This work is dedicated to her sacrifices over the years. iv TABLE OF CONTENTS ACKNOWLEDGMENTS ....................................................................................... i LIST OF FIGURES ............................................................................................. viii LIST OF TABLES................................................................................................. xi Overview..................................................................................................................1 Background .........................................................................................................1 The host-parasite system .....................................................................................3 Literature Cited..................................................................................................11 Chapter One: The role of non-odonate arthropods in the recruitment of Haematoloechus coloradensis and Haematoloechus complexus in newly metamorphosed northern leopard frogs, Rana pipiens, and Woodhouse’s toads, Bufo woodhousii ....................................................................................................20 Introduction.......................................................................................................22 Materials and Methods......................................................................................24 Haematoloechus coloradensis field studies................................................24 Haematoloechus coloradensis snail first intermediate host infections.......26 Haematoloechus coloradensis non-odonate arthropod second intermediate host infections.......................................................................27 Haematoloechus coloradensis frog definitive
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