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A Study of Dendrochirotid Sea Cucumbers with a Focus on Cucumaria Frondosa and Its Potential Use in Integrated Multi-Trophic Aquaculture

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A Study of Dendrochirotid Sea Cucumbers with a Focus on Cucumaria Frondosa and Its Potential Use in Integrated Multi-Trophic Aquaculture A study of dendrochirotid sea cucumbers with a focus on Cucumaria frondosa and its potential use in integrated multi-trophic aquaculture By © Jiamin Sun A thesis submitted to the School of Graduate Studies in partial fulfillment of the requirements for the degree of Doctor of Philosophy Department of Ocean Sciences Memorial University of Newfoundland St. John’s, Newfoundland and Labrador, Canada November 2019 i Abstract Sea cucumbers play fundamental roles in marine ecosystems, and they have long been commercially harvested for seafood. In light of stock declines worldwide, research on cold- water suspension-feeding species is expanding. This thesis explores two species from the North Atlantic. The first chapter validates an aging technique in Psolus fabricii, based on the growth rings found in its large calcareous dermal plates. Imaging of plates obtained from juveniles of known age confirmed the annual addition of a layer that extends the plate both vertically and horizontally, generating a pair of dark and light rings that can be used for aging. Wild individuals from shallow inshore areas were aged to a maximum of 28 years and their main morphometrics compared with age. The three other experimental chapters focus on Cucumaria frondosa, which has been commercially harvested for decades in North America and was identified as a potential candidate for aquaculture, especially as a biofilter in integrated multi-tropic aquaculture (IMTA). The locomotor and feeding behaviours, and microhabitat selection (spatial distribution) of C. frondosa in response to various environmental factors were investigated in the laboratory. Sea cucumbers moved away from static conditions and fled the strongest flows, and their tentacle deployment and insertion rates (i.e. feeding rate) increased with flow. The flow regime favoured by C. frondosa was 21-40 cm s-1. Individuals were overall more mobile during the night, whereas no feeding differences were detected between diurnal and nocturnal phases. Gradients in phytoplankton concentration modulated the deployment of feeding tentacles but did not trigger any displacement toward the food source. C. frondosa exhibited a clear preference for substrates composed of bare rocks and rocks with coralline ii algae and displayed a slight preference for darker substrate backgrounds. Finally, C. frondosa held in effluent water from salmon culture was determined to assimilate the waste, which modulated its biochemical composition; however, its health condition declined, suggesting that it cannot find appropriate or sufficient nutrients for growth and reproduction in these wastes. The findings presented here aim to improve our understanding of the biology and ecology of cold-water suspension-feeding sea cucumbers to guide and assist fisheries management and aquaculture development. iii Acknowledgement I want to use this space in my thesis to thank all the people that directly or indirectly helped me during the four years. First and foremost, I would like to thank my supervisor, Annie Mercier, and long-time lab collaborator Jean-Francois Hamel for their guidance, patience, encouragement, passion, and enormous hours of time. I learnt a lot from them, including the attitude towards research, how to design studies, and how to write a scientific paper, which will be very helpful for my future career. I also appreciated the insightful comments of my supervisory committee members, Shawn Robinson and Sherrylynn Rowe, and my thesis examiners, Chris Parrish, Chris Pearce and Matthew Slater. Many thanks as well to the staff of the Joe Brown Aquatic Research Building (JBARB) including Danny Boyce, Jennifer Monk, Denise Tucker, Jessica Fry, Kelsie Jeannot, and Jill Porter for giving me opportunities to learn about aquaculture of finfish. I would like to thank all the members of Mercier Lab: Guillaume Caulier, Emy Montgomery, Camilla Parzanini, Justine Ammendolia, Mattew Osse, Janet Ferguson-Roberts, Brittney Stuckless, Fanny Volage and MacGregor Parent for all the encouragement and help. Special thanks to Bruno Gianasi for helping with the experiment and writing. I would also like to thank the laboratory services technicians for experimental setup, and the field services for animal collections. Thanks to Jeanette Wells for her infinite patience and assistance in the lab, as well as to Allison Pye for technical support. This research was funded by the Canadian Centre for Fisheries and Innovation (CCFI), the Department of Fisheries and Aquaculture (DFA) of Newfoundland and Labrador and iv the Ocean Frontier Institute, through an award from the Canada First Research Excellence Fund. I received a doctoral fellowship from the China Scholarship Council. Finally, I want to thank my parents and friends for their continuous support, encouragement and understanding at the times. v Table of Contents Abstract ............................................................................................................................... ii Acknowledgement ............................................................................................................. iv Table of Contents ............................................................................................................... vi List of Tables ...................................................................................................................... x List of Figures .................................................................................................................... xi List of Appendices ........................................................................................................... xvi Co-authorship Statement ................................................................................................. xvii Chapter 1. General Introduction ......................................................................................... 1 1.1 Ecological and social values of sea cucumbers .......................................................... 2 1.2 Overview of focal species Cucumaria frondosa and Psolus fabricii ......................... 5 1.2.1 Biology and commercial exploitation of Cucumaria frondosa .......................... 5 1.2.2 Biology of Psolus fabricii ................................................................................... 7 1.3 Major gaps in knowledge ........................................................................................... 7 1.4 Main objectives and thesis structure .......................................................................... 9 1.5 References ................................................................................................................ 11 1.6 Figures ...................................................................................................................... 21 Chapter 2. Age determination in echinoderms: first evidence of annual growth rings in holothuroids ...................................................................................................................... 26 2.1 Abstract .................................................................................................................... 27 2.2 Introduction .............................................................................................................. 27 2.3 Material and methods ............................................................................................... 31 2.3.1 Collections and cultures .................................................................................... 31 2.3.2 Plate extraction and identification .................................................................... 32 2.3.3 Validation of annual ring deposition ................................................................ 33 2.3.4 Correlation between growth rings and other morphometrics ........................... 34 2.4 Results ...................................................................................................................... 35 2.4.1 Plate morphology and layered ring patterns ..................................................... 35 vi 2.4.2 Validation of annual ring deposition in juveniles of known age ...................... 36 2.4.3 Analysis of age-related metrics in juvenile, wild and deep-sea individuals ..... 37 2.5 Discussion ................................................................................................................ 38 2.6 Acknowledgements .................................................................................................. 44 2.7 References ................................................................................................................ 44 2.8 Figures ...................................................................................................................... 52 2.9 Supplementary Material ........................................................................................... 57 Chapter 3. Influence of flow on locomotion, feeding behaviour and spatial distribution of a suspension-feeding sea cucumber .................................................................................. 62 3.1 Abstract .................................................................................................................... 63 3.2 Introduction .............................................................................................................. 64 3.3 Materials and methods ............................................................................................. 67 3.3.1 Collection, holding and
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