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Download PARASITE METACOMMUNITIES ACROSS SCALES: TREMATODES IN THEIR FRESHWATER MOLLUSK HOSTS by Katherine Lee Dosch Richgels B.A. University of Wisconsin - Madison, 2005 A thesis submitted to the Faculty of the Graduate School of the University of Colorado in partial fulfillment of the requirement for the degree of Doctor of Philosophy Department of Ecology and Evolutionary Biology 2014 This thesis entitled: Parasite metacommunities across scales: trematodes in their freshwater mollusk hosts written by Katherine Lee Dosch Richgels has been approved for the Department of Ecology and Evolutionary Biology Pieter Johnson Valerie McKenzie Kendi Davies Brett Melbourne Elisabeth Root Date_______________ The final copy of this thesis has been examined by the signatories, and we Find that both the content and the form meet acceptable presentation standards Of scholarly work in the above mentioned discipline. iii Richgels, Katherine Lee Dosch (Ph.D., Ecology and Evolutionary Biology) PARASITE METACOMMUNITIES ACROSS SCALES: TREMATODES IN THEIR FRESHWATER MOLLUSK HOSTS Thesis directed by Associate Professor Pieter T. J. Johnson ABSTRACT Metacommunity theory investigates how local (species interactions and environmental filters) and regional (movement across the landscape) processes combine to determine the distribution, composition, and diversity of communities. In particular, studies of metacommunities usually explicitly or implicitly incorporate space, leading to an emphasis on spatial scale. Most metacommunity studies have focused on free-living organisms; however, using parasite communities offers unique insight into metacommunity patterns and processes through high replication and the ability to incorporate an additional scale. Complex life cycle parasite communities have three spatial scales that are biological important (1) within host, where parasite communities interact with each other and the host immune system, (2) within locality, where the host demography and environmental conditions can affect free-living parasite stage success, and (3) across the landscape, following the movement of their most vagile hosts, usually vertebrates. I used a metacommunity of flatworm (digenean trematode) parasites in their freshwater mollusk hosts to investigate metacommunity patterns and processes across scales. I used a combination of broad field surveys, advanced statistics, mathematical models, and experimentation to evaluate how patterns and processes affecting metacommunities shifted across the spatial scale of investigation. Within hosts, I found that parasite communities can be interactive, affecting each other’s colonization of host snails in controlled experimental mesocosms. Scaling up to within a locality, site and species specific feedbacks were more important than interspecific interactions based on a series of metacommunity models fit to a three year field dataset of a trematode metacommunity. On the same metacommunity scale, I investigated the relationship between avian hosts and trematode infections. I found that avian host use had strong seasonal patterns, and that trematode species richness and iv prevalence was positively related to the abundance and richness of birds. Then I scaled up again to consider patterns and processes affecting trematode metacommunities across the landscape using a two year field study. The availability of mollusk hosts was most important for landscape level trematode metacommunity structure. Overall, the drivers of parasite metacommunities shifted across scales, with interspecific interactions important within hosts, but with site level characteristics most important within sites and across the landscape. DEDICATION This thesis is dedicated to my parents, sisters, brothers, and husband, whose belief in me and endless support, love, and encouragement has provided the foundation for this achievement. vi ACKNOWLEDGEMENTS This thesis would not have been possible without the support and aid of numerous people. First, I would like to sincerely thank my thesis advisor, Dr. Pieter Johnson, who was an extraordinary mentor and friend. He led by example, always setting high standards in ethics, writing, and science, and expecting the same from me. In addition, he was always available for advice about personal, experimental, or scientific problems. By teaching me to think critically and scientifically, he has prepared me to be successful in my future career. I also greatly appreciate the diversity of projects, approaches, and collaborations he included me in, helping me to develop into a well-rounded and diverse scientist. I would also like to thank my thesis committee, Dr. Valerie McKenzie, Dr. Kendi Davies, Dr. Brett Melbourne, and Dr. Elisabeth Root, who have provided invaluable insight into difficult problems. Whether helping to develop mathematical models, grasp theoretical metacommunity concepts, or bolster my confidence, they have all contributed in a large way to my dissertation. I am grateful to the members of the Johnson Lab, Dr. Chelsea Wood, Dr. Bethany Hoye, Dr. Kimberly Medley, Dr. Jason Hoverman, Dr. Esra Kellermans, Dr. Brett Goodman, Dr. Sara Paull, Dr. Sarah Orlofske, Dan Preston, Joseph Mihaljevic, Max Joseph, Ian Buller, and Travis McDevitt-Galles, which have fostered a creative, collaborative, and friendly environment, often providing much needed advice and input on sticky problems in experimental design, data analysis, or presentation. Miranda Redmond, Jazzmin Jenkins, Bryan Lafonte, and Dain Calhoun have been superb lab managers, keeping the lab and all those in it running smoothly. Lastly, my dissertation work was vastly improved by the help of numerous undergraduate paid assistants and volunteers, including Michelle Baragona, Kendra Gietzen, Jeff McFarland, Hidde Snieder, Jayleen Garace, Sako Barbarian, Brian Sechler, Asher Straw, Kurt Zimmerman, Josue Loma, Brita Schneiders, Emma Gallagher, and Saren Ploen. I would like to acknowledge the numerous funding sources that made my dissertation possible. I was supported for three years on a national science foundation graduate research fellowship (NSF-GRFP), which allowed me to focus solely on research. I was generously supported by the department of ecology and evolutionary biology at the University of Colorado at Boulder through 5 teaching assistantships and vii three yearly research grants. I also received several small grants for research travel and supplies from the grants in aid of research program at Sigma Xi, the University of Colorado Natural History Museum Van Burt Riper award, and the United Government of Graduate Students travel grant. Lastly I received generous support from my advisor’s NSF grant (DEB 0841758) for summer field work and supplies. viii CONTENTS CHAPTER I. Integrating parasites into metacommunity theory…………………………………………..1 The metacommunity concept ….…………………………………………………….1 Importance of spatial scale ..………………………………………………………..2 Intricacies of incorporating parasites ………………………………………………3 Organization of the dissertation …………………………………………………….4 II. Infestation with an annelid ( Chaetogaster limnaei limnaei ) reduces infection by a trematode (Echinostoma trivolvis ) in a freshwater snail ( Helisoma trivolvis )…………………………..6 Abstract ………………………………………………………………………………6 Introduction …………………………………………………………………………..6 Methods ………………………………………………………………………………9 Results ………………………………………………………………………………..15 Discussion ……………………………………………………………………………18 III. Integrating metacommunity models with field-collected infection data to elucidate factors driving depauperate parasite communities…………………………………………………………....23 Abstract ………………………………………………………………………………23 Introduction ………………………………………………………………………….23 Methods ………………………………………………………………………………26 Results ………………………………………………………………………………..32 Discussion ……………………………………………………………………………39 Supplementary material ……………………………………………………………...45 IV. Use of small pond habitats by birds and its consequences for trematode infection in freshwater snails…………...……………………………………………..……………………………….50 Abstract ………………………………………………………………………………50 Introduction …………………………………………………………………………..51 Methods ……………………………………………………………………………….53 ix Results ………………………………………………………………………………...58 Discussion …………………………………………………………………………….62 Supplementary material ………………………………………………………………69 V. Evaluating the role of regional and local processes in structuring a larval trematode metacommunity of Helisoma trivolvis ………………………………………………………..73 Abstract ………………………………………………………………………………73 Introduction…………………………………………………………………………..74 Methods ………………………………………………………………………………76 Results ………………………………………………………………………………..83 Discussion …………………………………………………………………………….87 Supplementary material ………………………………………………………………91 VI. Conclusion……………………………………………………………………………………..93 Parasites in a metacommunity context ………………………………………………..93 Future directions ………………………………………………………………………94 Implications for the ecological context of disease …………………………………….95 REFRENCES…………………………………………………………………………………………..96 x TABLES Tables 2.1 Summary of the variables used in the analysis of Chaetogaster limnaei limnaei and Echinostoma trivolvis prevalence, infection success, and intensity……………………………………………15 2.2 Standardized coefficients with standard error for Echinostoma trivolvis and Chaetogaster limnaei limnaei prevalence, infection success, and intensity………..…………………………………..18 3.1 Description of the candidate models, including parameters, number of parameters, and main assumptions……………………………………………………………………………………....31 3.2 Observed infection prevalence for each parasite species by sampling date at Duck
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