THE ECOLOGY OF DEEP-SEA CHEMOSYNTHETIC HABITATS, FROM POPULATIONS TO METACOMMUNITIES A Dissertation Submitted to the Temple University Graduate Board In Partial Fulfillment of the Requirements for the Degree DOCTOR OF PHILOSOPHY by Alanna G. Durkin May 2018 Examining Committee Members: Erik E. Cordes, Advisory Chair, Biology Amy Freestone, Biology Rachel Spigler, Biology Amanda Demopoulos, External Member, United States Geological Survey © Copyright 2018 by Alanna G. Durkin All Rights Reserved ii ABSTRACT Chemosynthetic ecosystems are habitats whose food webs rely on chemosynthesis, a process by which bacteria fix carbon using energy from chemicals, rather than sunlight-driven photosynthesis for primary production, and they are found all over the world on the ocean floor. Although these deep-sea habitats are remote, they are increasingly being impacted by human activities such as oil and gas exploration and the imminent threat of deep-sea mining. My dissertation examines deep-sea chemosynthetic ecosystems at several ecological scales to answer basic biology questions and lay a foundation for future researchers studying these habitats. There are two major varieties of chemosynthetic ecosystems, hydrothermal vents and cold seeps, and my dissertation studies both. My first chapter begins at cold seeps and at the population level by modeling the population dynamics and lifespan of a single species of tubeworm, Escarpia laminata, found in the Gulf of Mexico. I found that this tubeworm, a foundation species that forms biogenic habitat for other seep animals, can reach ages over 300 years old, making it one of the longest-lived animals known to science. According to longevity theory, its extreme lifespan is made possible by the stable seep environment and lack of extrinsic mortality threats such as predation. My second chapter expands the scope of my research from this single species to the entire cold seep community and surrounding deep-sea animals common to the Gulf of Mexico. The chemicals released at cold seeps are necessary for chemosynthesis but toxic to non- adapted species such as cold-water corals. Community studies in this area have previously shown that seeps shape community assembly through niche processes. Using iii fine-scale water chemistry samples and photographic mapping of the seafloor, I found that depressed dissolved oxygen levels and the presence of hydrogen sulfide from seepage affect foundation taxa distributions, but the concentrations of hydrocarbons released from these seeps did not predict the distributions of corals or seep species. In my third chapter I examine seep community assembly drivers in the Costa Rica Margin and compare the macrofaunal composition at the family level to both hydrothermal vents and methane seeps around the world. The Costa Rica seep communities have not previously been described, and I found that depth was the primary driver behind community composition in this region. Although this margin is also home to a hybrid “hydrothermal seep” feature, this localized habitat did not have any discernible influence on the community samples analyzed. When vent and seep communities worldwide were compared at the family-level, geographic region was the greatest determinant of community similarity, accounting for more variation than depth and habitat type. Hydrothermal vent and methane seeps are two chemosynthetic ecosystems are created through completely different geological processes, leading to extremely different habitat conditions and distinct sets of related species. However, at the broadest spatial scale and family-level taxonomic resolution, neutral processes and dispersal limitation are the primary drivers behind community structure, moreso than whether the habitat is a seep or a vent. At more local spatial scales, the abiotic environment of seeps still has a significant influence on the ecology of deep-sea organisms. The millennial scale persistence of seeps in the Gulf of Mexico shapes the life history of vestimentiferan iv tubeworms, and the sulfide and oxygen concentrations at those seeps determine seep and non-seep species’ distributions across the deep seafloor. v ACKNOWLEDGMENTS My unending gratitude goes out to my advisor Erik Cordes and my committee members Amy Freestone, Rachel Spigler, and Amanda Demopoulos. I am forever indebted to these brilliant scientists for guiding my work, helping me reach my potential as a researcher, and most of all for believing that I could finish this project when I did not believe in myself. They have supported me with an endless supply of guidance and mentorship, and Erik has also demonstrated an endless supply of patience despite my best attempts to find its limit. Besides inspiring me to appreciate all that science has to offer, Erik also gave me one of the greatest gifts of my life: the opportunity to work at sea. Of those working at sea, I must first thank the crew members of the R/V Atlantis, R/V Pisces, and R/V Ronald Brown along with the vehicle teams that maintain and pilot the DSV Alvin, AUV Sentry, and ROV Jason II. Without their skillful efforts, the data in this dissertation would never have been collected! I am also extremely privileged to have collaborated with so many phenomenal scientists and engineers on cruises. Working together on a ship inevitably bonds people together, and everyone I have spent time with at sea taught me invaluable skills and encouraged me to soar ever higher in life. These people include but are not limited to Jennifer Le, Kris Krasnosky, Ian Vaughn, Caitlin Adams, Charlotte Seid, Ben Moran, Greg Rouse, Shana Goffredi, Victoria Orphan, Sean Mullin, Kat Dawson, Lily Simonson, Erin Henning, Rachel Simister, Helen White, Fanny Girard, Jennifer Vaccaro, Sean Kelley and Andy Billings. I also owe special thanks to anyone who has every measured or extracted a tubeworm! vi On land, Temple University has been a bastion of support in so many areas of my development. The biology department has always provided a welcoming atmosphere thanks not just to the faculty but also to the dedicated office staff that keep everything running and make sure the graduate students are taken care of. All of the members of the Cordes Lab have created an amazing team I was proud to be a part of. Jay Lunden, Andrea Quattrini, and Sam Georgian set the bar high for graduate student success and were always willing to lend a hand to help us achieve the same. I am so grateful to Danielle Deleo, Carlos Gomez, Alexis Weinnig, Steve Auscavitch, April Stabbins, and Veronica Radice for the companionship they brought to the lab to help me through difficult challenges. Besides my lab members, I was thrilled to learn alongside many other amazing fellow graduate students including but not limited to Nichole Rigby, Nicole Mazouchova, Janne Pfeiffenberger, Carlee MacPherson Cunningham, Sarah DeVaul Princiotta, Elizabeth Rielly, and Katharine Papacostas. During my time at Temple, I learned how to be an educator in addition to a researcher. Thank you to all those who taught me to teach, including Evelyn Vleck, Sheryl Love, Dan Spaeth, and the Center for the Advancement of Teaching. Outside of the biology department, I am thankful I availed myself to Temple’s other resources for graduate students through the writing groups and writing retreats offered by the Writing Center as well as the dissertation support group offered through Tuttleman’s Counseling Center. These places gave me the opportunity to exchange ideas and make lifelong friends across disciplines, including Diane Evitts, Margaret Janz, vii Leslie Allison, Amanda Milena Alvarez, Lorraine Savage, Brittany Webb, Diane Garbow, and my roommate Steffi Kasperek. Finally, I need to thank my family. Without my mom and dad encouraging me throughout my academic career to pursue my interests, I never would have made it this far. My mom Karen instilled in me a love of reading and language that made spelling hundreds of taxonomic names correctly the easiest part of my research, and I was able to absorb some of my dad Steve’s gifts for public speaking and presence in the classroom. My sister Katie has always been there for me, from when we explored the outdoors and collected bugs as children to all of her support as an adult. Moving to Philadelphia brought us closer together geographically and emotionally, and I can’t thank her enough for all the meals, kitten parties, and social support from her and her circle of friends and husband Scott! I must also thank my loving ex-husband John Opatz for the support he provided throughout all but the home stretch of my graduate education. I made it through many trying times thanks to the emotional support of all the animals in my life. Although I don’t own my own pets, I know an abundance of wonderful pet owners who let me borrow their animals! Thank you to everyone who has ever let me petsit for them, and thank you to the stray cats of Temple’s campus. This research would not have been possible without funding from the National Science Foundation, the Bureau of Ocean Energy Management, TDI Brooks International, NOAA’s Office of Ocean Exploration and Research and National Oceanographic Partnership Program, and of course Temple University, which funded me through teaching assistantships and the dissertation completion grant. viii TABLE OF CONTENTS Page ABSTRACT ....................................................................................................................... iii ACKNOWLEDGMENTS ................................................................................................