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ON the SUCCESS of the HADAL SNAILFISHES the Influence Of ON THE SUCCESS OF THE HADAL SNAILFISHES The Influence of Trophic Ecology, Life History, and Pressure Adaptation on Depth Zonation in the Planet’s Deepest-Living Fishes A Dissertation Submitted to the Graduate Division of the University of Hawai‘i at Mānoa in Partial Fulfillment of the Requirements for the Degree of DOCTOR OF PHILOSOPHY IN MARINE BIOLOGY MAY, 2017 By Mackenzie Gerringer Dissertation Committee: Jeffrey Drazen, Chairperson Brian Popp Allen Andrews Craig Smith Anna Neuheimer Keywords: hadal zone, Liparidae, otoliths, stable isotopes, enzymes, stomach contents analysis © Copyright 2017 – Mackenzie E. Gerringer All rights reserved. ii This dissertation is dedicated to the teachers who challenged and inspired me. iii ACKNOWLEDGEMENTS I would like to sincerely thank my advisor, Dr. Jeff Drazen, for his enthusiasm, support, and understanding throughout this process. Your unadulterated love for fish, your tireless passion for education, and your graceful work-life balance are inspiring. I express my gratitude to my committee members, Drs. Allen Andrews, Brian Popp, Craig Smith, and Anna Neuheimer, who have taught me so much, have provided fruitful insights and discussions on this work and on science, and have been highly supportive of my education. I also especially thank Dr. Paul Yancey for his mentorship, example, encouragement, and friendship over the years. Thank you for teaching me and believing in me, working with you has been a great joy. Science, especially hadal science, is by necessity highly collaborative and I am extremely grateful those with whom I have had the opportunity to work on this research. I thank those involved in the HADES program for all their hard work, without whom this research would not have been possible. I am very grateful for those that have set such a wonderful example of grace, kindness, and professionalism in research collaborations, particularly Bruce Mundy, Ashley Rowden, Adam Summers, Andrew Stewart, Malcolm Clark, Dmitri Davydov, and Gary Huss. My sincere thanks to Alan Jamieson for scientific insights, compelling discussions, and support. I also thank Thomas Linley, who has been a wonderful nemesis, collaborator, and friend, and has contributed so much to this research. I am extremely grateful for the support of the National Science Foundation Graduate Research Fellowship, as well as to the other agencies that made this work possible, including Schmidt Ocean Institute and NOAA. I would like to especially thank the captains and crews of the iv research vessels that have supported this research – of the R/Vs Kaharoa, Falkor, Thompson, Okeanos Explorer, Centennial, and Shinyo-maru. I extend my sincere gratitude to the administrative and support staff in the Oceanography Department who have been so kind and helpful facilitating this work, particularly Anne Lawyer, Phil Rapoza, Catalpa Kong, Kristin Momohara, and Pamela Petras. Kindest thanks also to Lindsay Root and Xuan Tran, Marine Biology Program Coordinators and Tasha Ryan, Fellowships and Professional Development Coordinator, for all their hard work and support. My deepest thanks to my family and friends for their love and support throughout my life. Thanks to the 2013 Marine Biology Cohort, the 2014 Friday Harbor Fish Class, and the members of the Drazen lab for their friendship and support, especially Astrid Leitner, Chris Demarke, and Kristen Gloeckler. I also thank my friends outside of science, for their encouragement, support, and humor, which have kept me grounded throughout this process. Thank you, Amanda Ziegler for being such a wonderful office mate and friend, and for your shared wit, wisdom, support, and coffee. My heartfelt thanks to Logan Peoples for your support, understanding, insights, and encouragement. Thank you, Madison Gerringer, my sister and friend, for your love and your laughter. Finally, I thank my parents, Teresa and Michael Gerringer, for teaching me the value of education, dedication, and pursuing your dreams. I am so lucky to be your daughter and so grateful for all your support and love. v ABSTRACT The snailfishes, family Liparidae (Scorpaeniformes), have found notable success in the hadal zone from ~6,000–8,200 m, comprising the dominant ichthyofauna in at least five trenches worldwide. The hadal fish community is distinct from the surrounding abyss where solitary, scavenging fishes such as rattails (Macrouridae), cutthroat eels (Synaphobranchidae), eelpouts (Zoarcidae), and cusk eels (Ophidiidae) are most common. Little is known about the biology of these deepest-living fishes, or the factors that drive their success at hadal depths. Using recent collections from the Mariana Trench, Kermadec Trench, and neighboring abyssal plains, this dissertation investigates the role of trophic ecology, pressure adaptation, and life history in structuring fish communities at the abyssal-hadal boundary. Stomach content and amino acid isotope analyses suggest that suction- feeding predatory fishes like hadal liparids may find an advantage to descending into the trench – where amphipods are abundant. More generalist feeders and scavengers relying on carrion, such as macrourids, might not benefit from this nutritional advantage at hadal depths. Hadal fishes also show specialized adaptation to hydrostatic pressure, as seen in metabolic enzyme activities. Maximum reaction rate of lactate dehydrogenases from hadal liparids increased under pressures of 600 bar, while in shallow-living fishes, this enzyme was pressure-inhibited. These types of pressure adaptation are necessary for fishes to thrive at hadal depths. Intraspecific activities of tricarboxylic acid cycle enzymes, considered proxies of metabolic rate and nutritional condition, increased with depth of capture in hadal snailfishes, further suggesting an advantage to snailfishes living deeper in the trench where food availability may be higher. Analysis of otolith growth zones support an additional hypothesis – snailfishes may be adapted to a seismically active, high- disturbance hadal environment by having relatively short life-spans that are on the order of fifteen vi years when compared to other deep-sea fishes. Additional aspects of hadal snailfish biology, including thermal histories, reproduction, swimming kinematics, and buoyancy strategies are explored and discussed. The taxonomic description of a newly-discovered hadal liparid from the Mariana Trench is also included. This study provides insight into the ecology and physiology of deep-dwelling fishes and provides new understanding of adaptations to life in the trenches. vii TABLE OF CONTENTS Acknowledgments.......................................................................................................................... iv Abstract ................................................................................................................................ vi List of Tables ................................................................................................................................ ix List of Figures ..................................................................................................................................x Chapter I ..................................................................................................................................1 Introduction: The hadal liparids Chapter II ................................................................................................................................13 Comparative feeding ecology of abyssal and hadal fishes through stomach content and amino acid isotope analysis Chapter III ................................................................................................................................49 Metabolic enzyme activities of abyssal and hadal fishes: pressure effects and a re- evaluation of depth-related changes Chapter IV ................................................................................................................................82 Life history of abyssal and hadal fishes from otolith growth zones and oxygen isotopes Chapter V ..............................................................................................................................123 Distribution, composition, and functions of gelatinous tissues in deep-sea fishes Chapter VI ..............................................................................................................................150 Pseudoliparis swirei: A newly-discovered hadal liparid (Scorpaeniformes: Liparidae) from the Mariana Trench Chapter VII ..............................................................................................................................177 Conclusions: On the success of the hadal snailfishes Appendix ..............................................................................................................................196 Supplementary tables and figures viii LIST OF TABLES 1.1. Global geographic and bathymetric distribution of hadal liparids............................................4 1.2. Global collections of hadal liparids by year .............................................................................6 2.1. Collection information for stomach contents and stable isotope analyses .............................19 2.2. Hadal liparid prey tables .........................................................................................................22 2.3. Prey tables for abyssal species ................................................................................................24
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