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Interactions Among Invasive Pacific Red Lionfish, Fish Parasites, and Cleaning Mutualisms Native to Atlantic Coral Reefs

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Interactions Among Invasive Pacific Red Lionfish, Fish Parasites, and Cleaning Mutualisms Native to Atlantic Coral Reefs AN ABSTRACT OF THE DISSERTATION OF Lillian J. Tuttle for the degree of Doctor of Philosophy in Zoology presented on May 27, 2016. Title: Interactions among Invasive Pacific Red Lionfish, Fish Parasites, and Cleaning Mutualisms Native to Atlantic Coral Reefs. Abstract approved: _____________________________________________________________________ Mark A. Hixon What makes invasive species successful, and how do they affect native populations and communities? I addressed these key questions in the context of the invasion of Atlantic coral reefs by Pacific red lionfish (Pterois volitans). To assess the role of parasites in contributing to the success of this invasion, I compared infection rates of lionfish with syntopic carnivorous fishes at multiple locations in both the invasive and native ranges of lionfish. Invasive Atlantic lionfish had extremely few parasites when compared both to native Pacific lionfish and to ecologically similar native Atlantic reef fishes. Such “enemy release” may help to explain this successful invasion if lionfish consequently allocate more energy to growth and reproduction than to costly immune defenses. With few parasites limiting them, lionfish may consume ecologically important species, including Elacatinus spp. cleaning gobies: ubiquitous, conspicuous fishes that remove ectoparasites from other reef fishes. Although juvenile lionfish ate cleaner goby (E. genie) during laboratory experiments, they quickly learned to avoid them, likely due to a previously undescribed skin toxin in these gobies. Field experiments further revealed no change in the survival and growth rates of newly recruited cohorts of the cleaner goby in the presence vs. absence of lionfish. However, lionfish caused declines in the densities of the most abundant facultative cleaner, juvenile bluehead wrasse (Thalassoma bifasciatum), and of transient fishes that are often cleaned while visiting coral patch reefs. Therefore, lionfish do not have uniformly negative effects on native species; distasteful to potential predators, the cleaner goby is among the remarkably few small fish to escape predation by lionfish. The continued presence of Elacatinus spp. cleaning gobies, the predominant cleaners on invaded reefs, should limit cascading effects of lionfish on other Atlantic coral-reef inhabitants. Nonetheless, given their broad and voracious appetites, invasive lionfish will likely continue to affect native reef communities via predation on other cleaners and ecologically important fishes. ©Copyright by Lillian J. Tuttle May 27, 2016 All Rights Reserved Interactions among Invasive Pacific Red Lionfish, Fish Parasites, and Cleaning Mutualisms Native to Atlantic Coral Reefs by Lillian J. Tuttle A DISSERTATION submitted to Oregon State University in partial fulfillment of the requirements for the degree of Doctor of Philosophy Presented May 27, 2016 Commencement June 2016 Doctor of Philosophy dissertation of Lillian J. Tuttle presented on May 27, 2016 APPROVED: Major Professor, representing Zoology Chair of the Department of Integrative Biology Dean of the Graduate School I understand that my dissertation will become part of the permanent collection of Oregon State University libraries. My signature below authorizes release of my dissertation to any reader upon request. Lillian J. Tuttle, Author ACKNOWLEDGMENTS I once read a quote, I’m not sure by whom, that likened science to a first-rate piece of furniture in a person’s “upper chamber,” but only if that person had common sense on the ground floor. To extend the metaphor, my advisor, Mark Hixon, has an incredibly well furnished upper chamber. It is full of empirical artwork hanging from theoretical walls, an experimental armoire, a very well organized bureau, and a set of the most comfortably logical armchairs encircling a banquet-sized round table at which his academic family sits. Luckily, he is also grounded by an enviable work ethic, a dedication to teaching, an insatiable curiosity, and an immense love and respect for the ocean. Most profound is his ability to inspire hope when confronted with the challenges facing our generation. I am fortunate to have spent the last 6 years learning from him what is means to be a scientist of conscience, and hope to continue many more years of fruitful collaboration. Mahalo nui loa ko’o kumu. I thank my committee for their support and insight at several key transitional phases in my doctoral career (in chronological order). Though no longer on my committee, Isabelle Côté was an inspiration from the beginning as an amazing scientist who happened to be an expert in cleaning goby mutualisms and invasive lionfish. On her recommendation, I studied the evolution of cooperation for my oral preliminary exam, and had no idea how fascinated I would become with that field! “Retired but not forgotten” from my committee is Paul Murtaugh, who in my humble opinion is a statistician of the highest order. In his office we were equals, planning the simplest and most elegant ways to test my hypotheses. He encouraged me to let my story shine through the data, not hide behind the analysis. Mark Novak is a scientist who I respected from the moment I met him – at his job interview at OSU! He is calm, approachable, and always asks the questions that get to the heart of every issue. I hope to collaborate on a project with him, one day soon. Jerri Bartholomew was the perfect grad rep, especially because she’s the only fish parasitologist on my committee! I enjoyed disease ecology seminars with her, and can’t wait to have her “buggy” insight at my defense. My new statistics advisor, Charlotte Wickham, has been a blessing in the final months of my degree. I thank her for her thoughtful feedback, patience, and artistic skills (!) that helped me to interpret the baffling beta- 3. Also new to my committee is Anna Jolles. She’s a talented disease ecologist who loves getting her hands dirty with fieldwork. I hope to follow her lead! Next, I’d like to pay homage to my brothers and sisters in arms (also in chronological order). Tim Pusack, from the moment I met you during my visit to Corvallis, I had you pegged as my future best friend. I’m glad I was right. I should write an entire chapter here about what an incredible example you have been to my cohort and me. I envy your ability to diffuse any tough situation with your smile and a few kind words, and cannot begin to live up to your standard as a hardworking and eloquent (yes, eloquent) scientist. I raise a glass of whiskey to you, my friend in high and low places. Kurt Ingeman, when I described you as a Norse god to a group of CEI interns who hadn’t yet met you, they didn’t know I wasn’t lying. Your heart and your scientific prowess match your stature. I’m so happy you didn’t let a silly little thing like tinnitus truncate your doctoral career – you deserve it and will make an excellent professor and advisor one day. I was nervous when I walked off that 10- person plane on Little Cayman. It was the beginning of a new chapter, literally (Chapter 2) and figuratively. I was met by the smiling faces of Casey Benkwitt and Tye Kindinger, two of the closest friends and colleagues I’ll ever have. We’ve done this entire PhD thing together, from beginning to end, and I’m still not sure how I managed to be the first to defend…guess I’m the Southern tortoise to your Yankee hare? Tye, I’m sure I’ll never live up to your incredible work ethic and leadership in the field, nor your “dead-eye” for lionfish and gorgeous presentation design. Casey, you’ve got one hell of a bright light shining through you that the whole world can see. You’ve got an equally bright future ahead of you. Thank you for inspiring me to be a better scientist, person, and competitor! Mark Albins, you are a trailblazer and a friend. Without you, we would have all floundered (pun!) a long time ago. Our dissertations were built on the foundation you laid as the King of Lionfish and the Keeper of Goals. Alex Davis, as a roommate and colleague you are second to none. Of all the field seasons (five!) we had together, I’m especially glad we shared that last one. You just need to learn how to control that (Cage) rage. Seriously. Steph Green, I feel like we’ve packed a life’s worth of friendship and science into our all-too-short time together. But I’m confident that we will collaborate for many years to come! Eric Dilley, Chapter 4 is dedicated to your enduring and painstaking sacrifices to the Rock Sound fish gods. Mahalo nui, hoa noho, and long live the ‘uhu. Last but not least is Erik Brush – finally! another Southerner in the lab – may your science always outpace your mosey, my friend. When it’s all said and done, I spent over 14 months of my doctorate immersed in fieldwork. That would not have been possible without an army of special people. The unending guidance and support of Kevin Buch, OSU’s dive safety officer, allowed me to feel safe and well prepared for the best and worst of fieldwork. Thank you to Emily Anderson, Kristian Dzilenski, and Allison Stringer – field assistants extraordinaire – and to Ashley Coke, Delaney Coleman, and Tayler Nichols who selflessly volunteered to torture themselves by watching long hours of tropical fishes halfway across the world. Thank you to Pat Lyons, court jester at Tomfoolery Cay. Thank you to the literally hundreds of staff members at the Perry Institute of Marine Science, the Central Caribbean Marine Institute, and the Cape Eleuthera Institute whose dedication to science, education, and conservation made them perfect hosts despite our intense demands on their resources and hospitality.
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