An Integrated Approach to Studying the Trophic Ecology of a Deep-Sea Faunal Assemblage from the Northwest Atlantic
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AN INTEGRATED APPROACH TO STUDYING THE TROPHIC ECOLOGY OF A DEEP-SEA FAUNAL ASSEMBLAGE FROM THE NORTHWEST ATLANTIC by © Camilla Parzanini A thesis submitted to the School of Graduate Studies in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Marine Biology Department of Ocean Sciences Memorial University September 2018 St. John’s, Newfoundland and Labrador, Canada Alla mia preziosa famiglia i Abstract Despite being the largest ecosystem on Earth, the deep sea is still poorly known. Since the study of food webs allows a better understanding of ecosystems, the current research aimed to provide new insights into trophic relationships and element cycling within a deep-water faunal assemblage sampled in deep-sea areas of eastern Canada (Northwest Atlantic). The faunal assemblage consisted of a broad array of deep-sea taxa (143 species representing 8 phyla) collected within a tight window in space and time (100 km radius, 7 days), but across a large depth range (~1000 m) off insular Newfoundland. Functional diversity was studied along the bathymetric gradient. The integrated use of stable isotope, lipid, elemental, morphometric, and gut content analyses was crucial in obtaining an overall picture of the food web analyzed. Specifically, two major trophic pathways were recognized within the faunal assemblage: a pelagic pathway, relying on sinking organic matter (OM) as the primary food source; and a benthic pathway, in which settled OM constituted the base. A key role in energy and nutrient cycling was highlighted for pelagic vertical migrators and deep-water benthic communities. Vertical migrators actively provide inputs of food to benthic communities; benthic communities bioaccumulate certain energetic and nutritive compounds, and transfer them along the food web. Moreover, type and amount of lipids reflected not only dietary sources, but also environmental conditions typical of the deep sea. Large proportions of wax esters detected in certain species likely provide them with long-term energy reserves in a food-depleted environment. In addition, while the unsaturation level of phospholipid fatty acids increased, sterols diminished along the bathymetric gradient. This finding was interpreted to reflect adaptations of deep-water organisms to cope with increasing pressure and decreasing temperature with depth. Lastly, a preliminary ii analysis of the literature showed the existence of latitudinal trends in the isotopic and fatty acid composition of deep-sea benthic organisms, which exhibited lower C isotope ratios and higher proportions of ω3 fatty acids at temperate and polar latitudes than at tropical ones. This investigation raises concerns about potential effects of global climate change on deep-water communities, and about standardizing analytical methods to enable comparisons. iii Acknowledgements Above all, I would like to thank both my supervisors, Annie Mercier and Chris Parrish, as well as Jean-François Hamel, who co-guided me in this research project. Thank you, Annie, Chris and J-F, not only for providing professional guidance and expertise throughout my PhD, but also for believing in me and providing support during both the toughest and the most satisfying moments of these past 4 years. I have learnt much from you all, from the academic to the personal level, and I will always be grateful for that. I would also like to acknowledge DFO staff, in particular Don Stansbury, Keith Tipple, Dwayne Pittman, Vonda Wareham, and Mariano Koen-Alonso for allowing me to join the crew on board the CCGS Teleost, and for their help with logistics and species identification. Thanks to Evan Edinger as a member of my Supervisory Committee. Thanks to Jeanette Wells for her infinite patience and assistance in the lab, as well as to Allison Pye for technical support. Thanks to Emy Montgomery for sample collection and, above all, for the friendship and support throughout these past years; as well as to Uxue Tilves, Nurgul Ӧzdemír, Laura Cárreon-Palau, Rénald Belley, and Anne Provencher for further assistance with sample collection and data analysis. Thanks to my lab mates Justine, Jenna, Maryam, Sean, Bruno, Jiamin, Janet, and Tomer for all the help and entertainment throughout these PhD years. Thanks to all the lovely people and new friends I met in St. John’s, in particular to Daria, Sebastien, Giorgio, Jacopo, Jess, Ania, Maria, Kristin, Boni, Natalia, and Priscillia. No matter where the future will take us, I will always have you all in my heart. Thanks to Jaqueline, Priscila, and Brianna: wonderful roommates and friends. Thanks to Niccolo’ iv and Nina, who first believed in me and encouraged me to undertake this PhD. A huge thanks to my parents, sister, and friends Stefania, Lidia, Nadia, and Davide for the great support and love from back home; despite all the tears every time I have had to take the plane back to Canada, I have made it through knowing you were always with me. “As for me, I am tormented with an everlasting itch for things remote. I love to sail forbidden seas, and land on barbarous coasts” Herman Melville v Table of Contents Abstract ........................................................................................................................................... ii Acknowledgements ...................................................................................................................... iv Table of Contents .......................................................................................................................... vi List of Tables .................................................................................................................................. x List of Figures............................................................................................................................... xii List of Abbreviations and Symbols ........................................................................................... xiv List of Appendices ....................................................................................................................... xv CHAPTER 1 : INTRODUCTION AND OVERVIEW ........................................... 1-1 The deep sea: main features ...................................................................................................... 1-2 Food webs and nutrient cycling ................................................................................................ 1-3 Analysis of food webs and trophic interactions ......................................................................... 1-5 Gut content analysis .................................................................................................................. 1-6 Bulk stable isotope analysis ...................................................................................................... 1-7 Lipid and fatty acid analysis ...................................................................................................... 1-8 Further analyses ..................................................................................................................... 1-10 Exploring functional diversity along a depth gradient .......................................................... 1-11 Study area .................................................................................................................................. 1-12 Objectives and chapter structure ............................................................................................ 1-13 References ................................................................................................................................. 1-16 Tables ......................................................................................................................................... 1-23 Figures ....................................................................................................................................... 1-25 Co-authorship statement .......................................................................................................... 1-27 CHAPTER 2 : TROPHIC ECOLOGY OF A DEEP-SEA FISH ASSEMBLAGE IN THE NORTHWEST ATLANTIC ........................................................................ 2-1 Abstract ........................................................................................................................................ 2-2 Introduction ................................................................................................................................. 2-3 vi Methods ........................................................................................................................................ 2-7 Sampling ................................................................................................................................... 2-7 Stable isotope analysis ............................................................................................................. 2-8 Gut content analysis ................................................................................................................ 2-12 Biological data and morphological analysis ............................................................................ 2-13 Statistical analysis ................................................................................................................... 2-14 Results ......................................................................................................................................