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The Role of Emerging Pathogens in Amphibian Population Declines: Experimental Evidence

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The Role of Emerging Pathogens in Amphibian Population Declines: Experimental Evidence AN ABSTRACT OF THE THESIS OF Natalie M. Hambalek for the degree of Master of Science in Zoology presented on May 17, 2016. Title: The Role of Emerging Pathogens in Amphibian Population Declines: Experimental Evidence Abstract approved: _____________________________________________________ Andrew R. Blaustein Rapid rates of biodiversity loss have supported the notion that Earth is experiencing a sixth major extinction event. The causes of worldwide biodiversity loss are multifaceted and context dependent. One of the most prominent groups experiencing population declines and extinctions are amphibians. Several pathogens and their associated diseases are especially significant contributors to amphibian population declines. These include the chytrid fungus, Batrachochytrium dendrobatidis, the related but highly divergent fungal pathogen, B. salamandrivorans, and ranaviruses. In Chapter 1, I summarize the life-history traits of these three amphibian pathogens. In Chapter 2, I present a synthesis of these three emerging infectious pathogens by assessing their broad effects on amphibian hosts as found in experimental studies. I also examined the interactive effects of these pathogens with other potential and known contributors of amphibian population declines that have been experimentally studied. Well-designed experimental studies are critical for understanding the impacts of disease. However, inconsistencies in experimental methodologies often hinder our ability to form valuable comparisons and conclusions. Chapter 2 highlights the importance of implementing standard experimental protocols and reporting. Furthermore, we emphasize the significance of investigating the roles of multiple environmental and anthropogenic stressors. The effects of B. dendrobatidis and ranaviruses on their hosts have been well documented but the effects of coinfection with these pathogens are poorly understood. In Chapter 3, I experimentally examined the effects of simultaneous and independent exposure of B. dendrobatidis and ranavirus on survival, growth, and activity levels in two amphibian host species, the Pacific treefrog (Pseudacris regilla) and the western toad (Anaxyrus boreas). I predicted that coinfection with Bd and Rv would have increased lethal and sublethal effects on hosts compared with hosts that were infected with one of the pathogens independently. The results showed antagonistic effects of concurrent exposure to B. dendrobatidis and ranavirus, with individuals exposed to only one pathogen exhibiting more lethal and sublethal effects compared to individuals exposed to both pathogens. These results support the proposition that the dynamics behind multiple pathogen exposure are complex and that one pathogen may mitigate the effects of another to induce response variation. ©Copyright by Natalie M. Hambalek May 17, 2016 All Rights Reserved The Role of Emerging Pathogens in Amphibian Population Declines: Experimental Evidence by Natalie M. Hambalek A THESIS submitted to Oregon State University in partial fulfillment of the requirements for the degree of Master of Science Presented on May 17, 2016 Commencement June, 2016 Master of Science thesis of Natalie M. Hambalek presented on May 17th, 2016 APPROVED: Major Professor, representing Zoology Chair of the Department of Integrative Biology Dean of the Graduate School I understand that my thesis will become part of the permanent collection of Oregon State University libraries. My signature below authorizes release of my thesis to any reader upon request. Natalie M. Hambalek, Author ACKNOWLEDGEMENTS I would first like to thank my advisor Andy Blaustein for his unwavering support, sense of humor, and guidance throughout the last few years. There is no way to fully express my gratitude for giving me this opportunity and challenging me to go above and beyond to become a well-rounded scientist and a balanced human being. I have been lucky to learn from him. I am also grateful for Kathy Blaustein for her support and kindness. Thank you to my amazing committee: Dave Stone, Jeri Bartholomew, and Lindsay Biga for their thoughtful advice and support. Jim Rivers, Michelle Hladik, and Kelly Smalling all provided invaluable perspective and support in the beginning of my graduate work. I am grateful for Dede Olson for her helpful advice regarding work and beyond. Jason Hoverman has been an amazing collaborator for my graduate thesis work. Cathy Law of STEM Academy has been an incredible source of encouragement. Working alongside her is something I will take away from my graduate career and I am looking forward to providing impactful service in my future. I am exceptionally grateful for my fellow Blausteinites, both past and present. Barbara Han, Steph Gervasi, Julia Buck, Paul Bradley, Tara Chestnut, John Romansic, Giselle Xie and Linsdsay are all amazing scientists and role models. I could not have made it through these years without the mentorship of Trang Dang and Jenny Urbina, my lab moms and friends. I will dearly miss working alongside Trang in our tiny Cordley office and sharing laughs with Jenny. They made the lab a welcoming place and I treasure the time we spent together. Cassie Nix, Carmen Harjoe, and Paul Synder made lab meetings and work fun throughout the ups and downs. I could not have gotten through the last few months of graduate school without jumping over the final hurdles with Delia Negru and I really cherish our friendship. Emily Reynolds, once a student of mine, now a fellow colleague, I will miss our conversations and laughs. Thanks to Elva Manquera for being the trustiest undergraduate lab assistant ever. I know you will go on to accomplish great things! I am incredibly thankful to have been supported through teaching assistantships throughout the years. I have learned immensely from Lori Kayes’ commitment to education and it has been a pleasure working alongside her, Bob Mason, and the rest of my fellow TAs. I also wanted to thank the undergraduate students that I have had the pleasure to work with over the years. I have learned as much from them as they have from me. The Zoology department has been a wonderful and constant source of support. Tara, Traci, Trudy, and Jane have been great to work with on logistical matters. I am also extremely grateful to those from my undergraduate career who were instrumental to helping me get to where I am now. Merith Weisman, Karin Jaffe, Derek Girman, Daniel Smith, Gary Cherr, Cynthia Boaz, and Nick Geist, their perspectives have influenced me to be the best I can be academically, professionally, and personally. I have the absolute BEST COHORT IN THE WORLD: Brian Tanis, Danielle Tom, David Taylor, Ian Morelan, Jenna Sullivan, Katie Dziedzic, Kyle Coblentz, Leah Segui, and Trevor Tivey. I am so grateful for the moments and adventures we have shared both in and outside of work. EBC forever and Gladiators for life. To my friends outside my cohort: Brianna Gil, Adam Karmally, Aurora Tivey, Shannon Hennessey, Danielle Marias, Cara Keegan, and Alana Rose, thank you for providing countless laughs, escapades, and encouragement during my time here. Katie, Aurora, Shannon, Emily, and Peregrin, I will miss our Monday nights more than you can imagine! A HUGE thank you to my family for their constant optimism and keeping me grounded. To my mom, Ani, and my sisters, Meaghan and Sabrina, for always being my #1 cheerleaders and my main source of motivation. My grandma Arsiné for being my best friend and never letting me forget who I am. Tristin, Devin, Dylan, Krysten, Hampo, Suzy, Patrick, Liza, and Brian, I love you all and your belief in me has kept me going. Thank you to Marabeth and Mohamed Karmally for providing continual guidance and advice throughout the years. My adorable felines, Callie and Beasley, have been the best soundboards and sources of comfort. Finally, thank you to my partner in life, Ali Karmally, for your understanding, compassion, and relentless support through this journey. There are no words that could come close to expressing how lucky I feel to have you by my side. Behind every able man, there are always. CONTRIBUTION OF AUTHORS Emily Reynolds assisted with data collection in Chapter 2 and experiment execution in Chapter 3. Jenny Urbina assisted with data collection and provided helpful editing for Chapter 3. Trang Dang offered perspective on Chapter 2 and assisted with Bd culture and inoculation for Chapter 3. Jason T. Hoverman offered perspective to Chapters 2 and 3 and provided ranavirus culture for the experiment in Chapter 3. Barbara Han provided significant insight to Chapter 2. Dede Olson was involved with the design and writing with Chapters 2 and 3. Andrew Blaustein assisted with design and writing and contributed to data interpretation and conclusions of all Chapters. TABLE OF CONTENTS Page CHAPTER 1: GENERAL INTRODUCTION……………………………………… 1 Batrachochytrium dendrobatidis……………..……………... 4 Batrachochytrium salamandrivorans………….….……….... 5 Ranavirus……………………………………………………. 6 CHAPTER 2: THE IMPACTS OF EMERGING INFECTIOUS DISEASES AND OTHER CO- FACTORS ON AMPHIBIANS: A REVIEW OF EXPERIMENTAL STUDIES Abstract……………………………………………………... 9 Introduction…………………………………........................ 10 Methods…………………………………………………….. 13 Results………………………………………...............……. 13 Discussion………………………………………………….. 34 CHAPTER 3: COMPLEX DYNAMICS OF TWO EMERGING PATHOGENS, BATRACHOCHYTRIUM DENDROBATIDIS AND RANAVIRUS, ON AMPHIBIAN HOSTS Abstract……………………………………………………... 63 Introduction…………………………………......................... 64 Methods…………………………………………………….
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