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Biodiversity and Food Web Patterns in the Deep Sea: Why

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Biodiversity and Food Web Patterns in the Deep Sea: Why BIODIVERSITY AND FOOD WEB PATTERNS IN THE DEEP SEA: WHY FOOD QUALITY MATTERS by © Neus Campanyà i Llovet A Thesis submitted to the School of Graduate Studies in partial fulfillment of the requirements for the degree of Doctor of Philosophy Department of Biology Memorial University of Newfoundland July 2018 St. John’s Newfoundland and Labrador Abstract Despite multiple drivers of ocean change, few studies have addressed the role of food quality in structuring deep-sea benthic communities and food webs, and therefore its role in ecosystem processes (functioning). Based on a review of published data, I showed that food quality (i.e., nitrogen, pigment, lipid, carbohydrate, protein content) alters marine trophic guild composition, and thus food web structure, differently. In sampling heterogeneous submarine canyon and chemosynthetic ecosystems as model environments for food web and biodiversity studies, I found that patchy food quality distribution in Barkley submarine canyon influenced macroinfaunal community structure more strongly at smaller spatial scales (10’s of m), whereas major stressors (i.e., oxygen/depth) acted over larger scales (100’s of m). Increased food patchiness at a hydrate outcrop site (Barkley Hydrates), compared to sites located 20 and 600 m away, was related to increased macroinfaunal trophic diversity. Food quality explained substantial variation (~ 33 %) in macroinfaunal community structure, but H2S toxicity likely explained much of the remaining variation. Increasing spatial resolution of analysis (i.e., ≤ 10 m) indicated a 9-15 m influence radius around the most methane-active site (i.e., more depleted δ13C, indicative of chemosynthesis). Macroinfaunal total abundance at Barkley Hydrates tracked temporal changes in chemosynthetic organic matter, however, some taxa (i.e., Ampharetidae) apparently matched recruitment to phytodetrital pulses, much like the background community. An in situ enrichment experiment demonstrated modest differences in infaunal community species and functional trait composition in food patches enriched with either Chaetoceros calcitrans (a diatom) or Nannochloropsis 1 oculata (a lipid rich eustygmatal alga). Megaepifaunal visits to the enrichment patches increased in N. oculata over the first two weeks of the experiment, perhaps responding to increased abundance of potential infaunal prey. This research demonstrates a structuring role for food quality both in benthic communities and in food webs, with different effects on organisms of different sizes (e.g., macrofauna and megafauna). 2 Acknowledgements This work would not have been possible without the help and support of many scientists, colleagues, friends, and family members, who deserve a few lines in this thesis. I will start by thanking my supervisor, Dr. Paul Snelgrove, not only for this PhD opportunity that included cruises, conferences, and a constant development as a scientist, but for encouraging the pursuit of my own research questions. I would also like to give a special thanks to all of my committee members, Dr. Chris Parrish for his guidance on my first steps into the lipids world, his contribution to the second chapter of my thesis, and inmediate feedback on all my thesis chapters. I appreciate the detailed input on each chapter and committee meetings from Dr. Anna Metaxas, as well as her invitation to discuss my results with her lab members in Halifax. I thank Dr. Kim Juniper for the cruise opportunities with Ocean Networks Canada at Barkley Canyon, welcoming me and helping me on my first research cruise on board the R/V Falkor, and his valuable input during all of my committee meetings. Last but not least, I thank Dr. Annie Mercier for her input on my manuscripts and committee meetings. I also acknowledge valuable inputs from Drs. Suzanne Dufour and Evan Edinger for their inputs on earlier versions of the second chapter of my thesis through my comprehensive examination, and the anonymous reviewers who provided input on the chapters already submitted (2-5). A very generous thank to all the people that helped in the sample collections, starting from Drs. Marjolaine Matabos and Fabio de Leo for their consideration of my sampling needs when organizing scientific tasks on cruises to Barkley Canyon, followed by the 1 R/V Falkor and CCG Tully captains and crew, ROVs ROPOS and OE teams, and the principal investigator of the expeditions (Dr. Kim Juniper). A special thanks to Dr. Ursula Witte as well, from whom I borrowed the OceanLab spreaders without which the enrichment experiment (Chapter 6) would have not been possible. I thank Karen Douglas and Dr. Fabio de Leo for their assistance in data acquisition from Ocean Networks Canada, in particular the bathymetric rasters from Barkley Canyon, which helped understand the canyon topography. Along the same lines I thank Dr. Charlie Paull and Krystle Anderson from MBARI for providing a high-resolution AUV bathymetric raster from Barkley Hydrates, again used in this thesis to understand the topography of this chemosynthetic environment. I finally want to thank Drs. Rodolphe Devillers and Evan Edinger for their teaching and support on the very appealing world of topography and habitat mapping. I thank fellow lab members that provided help on cruise preparation and data analysis, in particular on the early stages of my PhD. Christine Vickers for her support and help in preparation for cruises, and Drs. Renald Belley, Chih-lin Wei, and Ryan Stanley for their input, motivation, and help on data analysis. Jeannette Wells for her teaching on laboratory techniques in the lipids lab and Alyson Pie for her help with stable isotope analysis. I also thank Dr. Shawn Leroux, not only for his advice on statistical analysis every time I hit a wall, but also for his motivation and invitation to lab meetings. I finally thank all the MUCEP and WISE students that came to the Snelgrove lab and helped in the preparation of samples and sediment sorting for posterior taxonomy. 2 Funding was provided by NSERC Discovery Grants to Dr. Paul Snelgrove and a fellowship Memorial University’s School of Graduate Studies. Travel to conference, meetings, and workshops were provided by Memorial University’s School of Graduate Studies, Ocean Networks Canada, and Deep-Sea Biology Society. I also offer special thanks to my family. A la meva parella, Javier Jaso, li agraeixo la paciència i el support incondicional donat durant tots aquests anys, també agraeixo als meus pares, la Mercè i el Joaquim, tots els recursos, educació i suport en les decisions preses sense els quals no podria haver completat aquest doctorat. Finalment reconèixer lo afortunada que sóc de tenir els germà/germanes que tinc, l’Eva, el Joan i la Maria, que tot i la distància són una font d’alegria i companyia. Us dedico a tots vosaltres aquest treball, especialment a la mare, i sense oblidar els nouvinguts (més o menys recents) a la familia, l’Anna, el Marc i el petit Brendan. 3 Table of contents Abstract ................................................................................................................................ 1 Acknowledgements .............................................................................................................. 1 Table of contents .................................................................................................................. 4 List of Tables ....................................................................................................................... 9 List of Figures .................................................................................................................... 12 List of common nomenclature and abbreviations .............................................................. 20 List of appendices .............................................................................................................. 20 Co-authorship statement .................................................................................................... 24 1. Introduction and overview .......................................................................................... 25 1.1. References........................................................................................................ 29 2. Rethinking the importance of food quality in marine benthic food webs .................. 33 2.1. Abstract ................................................................................................................... 33 2.2. Introduction ............................................................................................................. 34 2.3. What is food quality? .............................................................................................. 36 2.4. Methodology ........................................................................................................... 38 2.5. Results and discussion ............................................................................................. 41 2.5.1. Food availability to benthic ecosystems: Quantity vs quality .......................... 41 2.5.2. Importance of food quality in ecosystems with contrasting primary productivity ................................................................................................................. 52 2.6. Implications ............................................................................................................. 66 2.6.1. Ecosystem services and functions .................................................................... 66 2.6.2. Future
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