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Factors Influencing Infectious Agent Communities and Infection Burden in Free-Ranging Migratory Adult Salmonids Across Canada

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Factors Influencing Infectious Agent Communities and Infection Burden in Free-Ranging Migratory Adult Salmonids Across Canada Factors Influencing Infectious Agent Communities and Infection Burden in Free-Ranging Migratory Adult Salmonids Across Canada by Jacqueline M. Chapman A thesis submitted to the Faculty of Graduate and Postdoctoral Affairs in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Biology Carleton University Ottawa, Ontario © 2020 Jacqueline M. Chapman Dedication In loving memory of Ursula “Sula” Ward (Grannie) and Dr. Lt. Colonel George Robert Irvin Power (Dindin), both of whom passed during the course of this research. Each shared with me their insatiable curiosity, love of family, and provided unwavering support that I will carry with me always. ii Abstract While the importance of disease-induced mortality in wild fish populations has been purported, little research has investigated infectious agent dynamics in free-ranging fishes. The objective of this thesis was to investigate host-pathogen dynamics in three ecologically, culturally, and economically important salmonid species to characterize biological and environmental factors that mediate host response and survival associated with relative infection burden (RIB). To achieve this goal, a synthesis of the current state of wild fish epidemiology was conducted, with a focus on novel genomic techniques and ways in which they can be used to complement commonly employed fisheries field methods. High throughput qPCR and non-lethal gill biopsies were then used in three separate field studies to investigate RIB of microbial infectious agents and genetic biomarkers of host condition. To characterize the transcriptomic response of a long-lived, iteroparous salmonid to infectious agents and investigate the potential for invasive pathogens in Arctic waters, Arctic char from three separate populations were sampled during the fall migration, revealing site-specific differences in pathogen species richness and RIB, and provided new records for detection of likely endemic infectious agents. To investigate the influence of high water temperatures, Atlantic salmon were experimentally displaced downstream of a barrier and periodically sampled to track changes in infectious agent prevalence, relative infection burden, and host response over a 32 day period. Here, river temperature was significantly related to stress and immune biomarkers, while RIB was negatively associated with body condition. Finally, radio telemetry was used to track post-release survival and behaviour of coho salmon exposed to experimental fisheries stressors to characterize interactions between fisheries stress, iii host condition, and RIB. Fishery treatment and RIB were not associated with survival, however RIB was associated with post-release behaviour in that high RIB began up-river migration post-release sooner than fish with lower RIB. The duration of handling alone was significantly related to mortality irrespective of fisheries treatment. Together, these findings demonstrate the diversity of factors associated with infectious agent communities and host response and provide valuable information for the ongoing monitoring and investigation of wild salmonids. iv Acknowledgements Throughout my graduate studies I have been extremely fortunate to work with Dr. Steven Cooke and the incredibly talented students, managers, and technicians that have made up the Fish Ecology and Conservation Physiology Lab over the years. The collaborations and friendships that I have made over the last several years have and will continue to be inspirational and I look forward to working with many current and past colleagues in the future. I am especially grateful to A. Teffer, V. Nguyen, J. Brooks, G. Raby, R. Anderson, K. Cook, J. Brownscombe, and C. Hatry, all of whom provided support, lively discourse, and many laughs over the years. Endless thanks are given to T. Ward, who provided support during all facets of this process. The challenges associated with holding three separate field seasons in three unique and disparate locations required the support, guidance, and assistance of many. In British Columbia, I am especially thankful to all those who participated in field work on the Fraser River, especially D. Patterson, K. Robinson, A. Teffer, K. Cook, A. Bass, A. Lotto, P. Szekeres, L. Elmer, and C. White. I am also grateful to the Kwantlen First Nation for allowing this research to take place on their lands. In Cambridge Bay, I am grateful to R. Lennox and D. Struthers for their fishing expertise, persistence, and patience, and to L. Harris and B. Malley from Fisheries and Oceans, Jimmy and Ruby Haniliak, Anne Isnor, the Ekaluktutiak Hunters and Trappers Organization board members, and the community of Cambridge Bay for their logistical support, guidance, warm welcome to the community and support for this research. In Newfoundland, I am thankful for the guidance and logistical support received from M. Robertson and staff at the Fisheries and Oceans Campbellton River counting fence, and to R. Lennox and W. v Twardek for their assistance in the field. I am eternally grateful for the expertise that K. Miller, S. Li, K. Kaukinen, A. Schultz, and T. Ming shared at the Molecular Genetics Laboratory. Their eternal patience fielding never-ending questions and trouble-shooting through failed assays and temperamental liquid handlers is truly what made this thesis possible. vi Preface All research presented in this thesis was conducted in accordance with animal care protocols in accordance with guidelines put forth by the Animal Care Council of Canada and approved by committees at Carleton University, the University of British Columbia, and Fisheries and Oceans Canada. All animal collection was done under federal scientific collection permits administered by the Department of Fisheries and Oceans Canada. Thesis Format This thesis is presented in manuscript-based format. In an effort to maintain clarity, as there are subtle differences in methods in each data chapter, I have left the detailed description of laboratory methods in each chapter, resulting in repetition of certain sections. Acknowledgements for each data chapter have been included in the thesis acknowledgement section. vii Chapter 2: Disease ecology of wild fish: Opportunities and challenges for linking infection metrics with behaviour, condition, and survival. Chapman, JM, Teffer, AK, Kelly, L, Miller, KM, Cooke, SJ. The idea for this paper was conceived by Chapman with contribution from Cooke, Teffer, and Kelly. A version of this paper was presented at the American Fisheries Society Conference in August 2018 by Teffer in lieu of Chapman’s attendance. Another version of this paper was presented at the International Conference of Fish Telemetry by Chapman in June 2019. This manuscript is in prep for submission to Fisheries Research. Chapter 3: A survey of microbial infectious agents and characterization of immune response in adult migratory Arctic char (Salvalinus arcticus) intercepted during fall migration in three watersheds in the Kitikmeot region of Nunavut, Canada. Chapman, JM, Lennox, RL, Struthers, D, Malley, B, Harris, L, Miller, KM, Cooke, SJ. This study was designed by Chapman and Cooke with data collection and field support from Lennox, Struthers, Malley, and Harris. Laboratory analyses were conducted by Chapman with support from Miller. Chapman analyzed the data and wrote the paper, which is currently in prep for submission to the Journal of Fish Diseases. viii Chapter 4: Changes in the condition, infectious agents, and transcription profiles of wild Atlantic salmon during up-river migrations Chapman, JM, Lennox, RL, Twardek, W, Robertson, M, Miller, KM, Cooke, SJ. This study was designed by Chapman, Robertson, Cooke, and Lennox with data collection and field support from Lennox and Twardek. Robertson provided equipment and logistical support. Laboratory analyses were conducted by Chapman with support from Miller. Chapman analyzed the data and wrote the paper, which is currently in prep for submission to the Canadian Journal of Fisheries and Aquatic Sciences. Chapter 5: Handling, infectious agents, and physiological condition influence survival and post-release behaviour in migratory adult coho salmon after experimental displacement Chapman, JM, Teffer, AK, Bass, AL, Hinch, SG, Patterson, DA, Miller, KM, Cooke, SJ. 2020. Handling, infectious agents, and physiological condition influence survival and post-release behaviour in migratory adult coho salmon after experimental displacement. Conservation Physiology 10.1093/coaa033. This study was designed by Chapman, Cooke, Hinch, and Patterson. Chapman collected the data with significant contribution from Bass and Teffer. Hinch, Patterson and Cooke provided equipment. Bass and Teffer contributed to data processing. Chapman conducted laboratory analyses with support from Bass, Teffer, and Miller. Chapman analyzed the data and wrote the paper. ix Table of Contents Abstract .............................................................................................................................. ii Acknowledgements ........................................................................................................... v Preface .............................................................................................................................. vii List of Tables .................................................................................................................. xiii List of Figures ................................................................................................................
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