ENVIRONMENTAL & PHYSIOLOGICAL INFLUENCES ON THE BEHAVIOUR AND SURVIVAL OF ADULT SOCKEYE SALMON DURING THEIR COASTAL MIGRATION by Stephen Matthew Drenner B.A., Texas Christian University, 2006 M.Sc., Texas Christian University, 2008 A THESIS SUMBITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY in The Faculty of Graduate and Postdoctoral Studies (Forestry) THE UNIVERSITY OF BRITISH COLUMBIA (Vancouver) July 2015 © Stephen Matthew Drenner, 2015 ABSTRACT The reproductive migration of anadromous salmon through coastal waters is among the most challenging phases of their life cycle, yet our understanding of the mechanisms underlying this migration is limited. Thus, the objective of this thesis was to develop a better understanding of how environmental conditions and fish physiologic state influence behaviour and survival of homing anadromous salmon in coastal waters. Using a literature synthesis, I identified consistent behaviours across anadromous salmon species and life stages in marine waters including diel patterns and consistent swimming speeds. I further identified critical knowledge gaps, including a need for synchronized study of both environmental and physiological conditions. In field studies, I combined thermal data loggers, biotelemetry and physiological sampling and found that homing sockeye salmon exhibited diel and variable thermal experiences (8.4 °C to 20.5 °C) in coastal waters, potentially related to gaining cues for navigation. Sockeye salmon tended to follow coastlines and migration rate was related to wind patterns, salinity and fish physiological state. I propose that wind-induced currents exposed sockeye salmon entering the estuary to stronger olfactory cues associated with freshwater, which resulted in faster migration rates due to increased navigation ability or advanced reproductive maturity through a neuroendocrine response. Once migration neared freshwater, sockeye salmon used wind-induced currents to aid in movements, which may be associated with energy conservation. I further identified a genomic signature related to marine survival, which was associated with stress, immune response, metabolic processes, protein biosynthesis and osmoregulation. This genomic signature was similar to that identified in a previous study ! ""! examining freshwater survival, but with an opposite relationship with survival, which I attribute to the attenuation of disease resistance of fish upon exposure to elevated river temperatures. Through the use of multiple research approaches, this thesis advances the biological understanding of the marine homing migration of sockeye salmon by empirically establishing novel relationships between environmental conditions, physiological state and sockeye salmon behaviour and survival in marine waters. In addition, this thesis is broadly applicable to other anadromous salmon, as well as to studies invoking a similar approach of physiological biotelemetry for studying animal movements. ! """! PREFACE Chapter 2: A synthesis of tagging studies examining the behaviour and survival of anadromous salmonids in marine environments Authors: SM Drenner, TD Clark, CK Whitney, EG Martins, SJ Cooke, SG Hinch. Journal: PLoS ONE 2012 7(3): e31311. doi:10.1371/journal.pone.0031311 Status: Accepted 01/05/2012 Comments: This study was conducted, analyzed and written by SMD under supervision of TDC, SGH, SJC. EGM and CKW provided reviewing and editing assistance. SGH, TDC and SJC provided insight on study design. Chapter 3: Variable thermal experience and diel thermal patterns of homing sockeye salmon in coastal marine waters Authors: SM Drenner, SG Hinch, EG Martins, D Robichaud, TD Clark, LA Thompson, DA Patterson, SJ Cooke, RE Thomson Journal: Marine Ecology Progress Series 2014 496: 109-124 Status: Accepted 09/03/2013 Comments: This study was conducted, analyzed and written by SMD under supervision of SGH, and RET. EGM provided analysis support, TDC and DR provided field assistance, and LAT and DAP provided laboratory support. SGH, EGM, TDC, DAP, SJC and RET provided insight on study design and interpretation. ! "#! Ethics Approval: This research was approved by the University of British Columbia Animal Ethics Committee (animal care permit: A08-0388 )in accordance with the Canadian Council on Animal Care. Chapter 4: Environmental conditions and physiological state influence estuarine behaviour of homing sockeye salmon. Authors: SM Drenner, SG Hinch, EG Martins, NB Furey, TD Clark, SJ Cooke, DA Patterson, D Robichaud, DW Welch, AP Farrell, RE Thomson Journal: Fisheries Oceanography Status: Accepted 04/28/2015 Comments: This study was conducted, analyzed and written by SMD under supervision of SGH. EGM and NBF provided analysis support. TDC provided field assistance, and SGH, EGM, NBF, TDC, SJC, DAP, DR, DWW, APF and RET provided insight on study design and interpretation. Ethics Approval: This research was approved by the University of British Columbia Animal Ethics Committee (animal care permit: A08-0388) in accordance with the Canadian Council on Animal Care. Chapter 5: Transcriptome patterns and blood physiology associated with homing sockeye salmon fate during final stages of marine migration Authors: SM Drenner, SG Hinch, NB Furey, TD Clark, S Li, T Ming, KM Jeffreis, DA Patterson, SJ Cooke, D Robichaud, DW Welch, AP Farrell, KM Miller Status: In prep ! #! Comments: This study was conducted, analyzed and written by SMD under supervision of SGH, and KMM. TDC provided field assistance. DAP, SL and TM provided laboratory analysis. NBF provided analysis assistance and edits. SGH, KMM, TDC, SJC, DAP, DR, DWW, and APF assisted with study design and interpretation. Ethics Approval: This research was approved by the University of British Columbia Animal Ethics Committee (animal care permit: A08-0388) in accordance with the Canadian Council on Animal Care. ! #"! TABLE OF CONTENTS ABSTRACT....................................................................................................................... ii! PREFACE......................................................................................................................... iv! TABLE OF CONTENTS ............................................................................................... vii! LIST OF TABLES ............................................................................................................ x! LIST OF FIGURES ........................................................................................................ xii! LIST OF ABBREVIATIONS ....................................................................................... xiv! ACKNOWLEDGEMENTS .......................................................................................... xvi! DEDICATION .............................................................................................................. xvii! CHAPTER 1: INTRODUCTION.................................................................................... 1! 1.1 Animal migrations .................................................................................................... 1! 1.2 Reproductive migrations of anadromous salmon ..................................................... 7! 1.2.1 Anadromous salmon background ...................................................................... 7! 1.2.2 Reproductive maturation ................................................................................... 8! 1.2.3 Homing............................................................................................................... 8! 1.2.4 Osmoregulation................................................................................................ 10! 1.2.5 Energetics ........................................................................................................ 12! 1.2.6 Stress................................................................................................................ 13! 1.2.7 Coastal and estuarine environment ................................................................. 14! 1.3 Physiological biotelemetry...................................................................................... 16! 1.4 Thesis objectives and chapter overview ................................................................. 17! CHAPTER 2: A SYNTHESIS OF TAGGING STUDIES EXAMINING THE BEHAVIOUR AND SURVIVAL OF ANADROMOUS SALMON IN MARINE ENVIRONMENTS ......................................................................................................... 21! 2.1 Introduction............................................................................................................. 21! 2.1.1 Importance of salmon, and recent population trends ...................................... 21! 2.1.2 Objectives of this review .................................................................................. 23! 2.1.3 Life histories of salmon.................................................................................... 24! 2.1.4 Overview of tagging technologies and techniques........................................... 25! 2.2 Methods................................................................................................................... 27! 2.3 Results & discussion............................................................................................... 28! 2.3.1 General observations....................................................................................... 28! 2.3.2 Life-stage specific observations......................................................................