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Habitat Preferences and Fitness Consequences for Fauna Associated with Novel Marine Environments

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Habitat Preferences and Fitness Consequences for Fauna Associated with Novel Marine Environments Habitat preferences and fitness consequences for fauna associated with novel marine environments Luke T Barrett orcid.org/0000-0002-2820-0421 Submitted in total fulfilment of the requirements of the degree of Doctor of Philosophy September 2018 School of BioSciences University of Melbourne ABSTRACT The rapidly expanding reach of anthropogenic environmental change means that animals must now navigate landscapes comprised largely of modified and degraded habitats. Individuals that correctly perceive habitat quality will be best placed to survive and reproduce in novel environments, but where environmental change outpaces the evolution of behavioural responses, mismatches can arise between cues and the underlying value of habitats. These mismatches can lead individuals to select habitats that offer relatively poor fitness outcomes, creating ecological traps. In environments where ecological traps are likely to occur, data on habitat preferences and fitness consequences can fundamentally change predictions of metapopulation models and increase our understanding of the role that novel habitats play in population persistence, but such data are rarely collected. In this thesis, I first conduct a global meta-analysis to assess the state of knowledge on habitat preference and fitness metrics in animal populations, using wildlife populations associated with aquaculture as a case study. My findings reveal that responses to aquaculture vary widely across taxa and farming systems, ranging from large increases in abundance to near complete displacement. However, the influence of aquaculture on wildlife populations remains poorly understood, as researchers rarely obtain appropriate measures of habitat preference, survival or reproductive success. Accordingly, in subsequent chapters I apply the ecological trap framework to assess marine habitats modified by aquaculture or invasive species. In the first application, I collect wild Atlantic cod (a species known to be attracted to salmon farms) from areas of high and low salmon farming intensity, and compare reproductive fitness via a captive spawning trial with hatchery-rearing of offspring. I found limited negative effects of high farming intensity on quality of offspring. In the second application, I show that the threat of predation by a native keystone predator may limit the ability of an invasive seastar to exploit a food-rich habitat at shellfish farms. In the third application, I show that an invasive canopy-forming marine macroalga provides viable habitat for native fishes and may help to maintain fish biodiversity in areas where urban impacts have driven a decline in native macroalgal canopy cover. Together, this thesis demonstrates the utility of individual-level data on habitat preference and fitness outcomes— via the application of the ecological trap conceptual framework—in assessing the impacts of novel habitats on animals, and recommends greater use of this approach in future investigations into the impacts of human-induced rapid environmental change in coastal marine ecosystems. i DECLARATION This is to certify that: The thesis comprises only my original work towards the PhD except where indicated in the Preface. Due acknowledgement has been made in the text to all other material used. The thesis is fewer than 100 000 words in length, exclusive of tables, maps, bibliographies and appendices. Luke Barrett September 2018 Cover image: Mesocosm reef stocked with invasive wakame kelp (Undaria pinnatifida) ii PREFACE I am the primary author and principle contributor on all chapters presented in this thesis. My supervisors, Stephen E Swearer and Tim Dempster, are co-authors on all chapters. Article publication status and author contributions Chapter Two: Published by Reviews in Aquaculture on 14 Aug 2018. Co-authored by Tim Dempster and Stephen E Swearer. LTB, TD and SES conceived and designed the experiment; LTB conducted the experiment and collected data with assistance from technical staff and volunteers; LTB analysed the data and wrote the manuscript; TD and SES provided editorial comments. Contributions: LTB 80 %, TD 10 %, SES 10 % Chapter Three: Published by Aquaculture Environment Interactions on 16 Aug 2018. Co- authored by Tim Dempster, Stephen E Swearer, Ørjan Karlsen, Torstein Harboe and Sonnich Meier. LTB, TD, SES, ØK and TH conceived and designed the experiment; LTB conducted the experiment and collected data with assistance from ØK, TH and SM, as well as technical staff at the Norwegian Institute of Marine Research; LTB analysed the data and wrote the manuscript; TD, SES and SM provided editorial comments. Contributions: LTB 75 %, TD 5 %, SES 5 %, ØK 5 %, TH 5 %, SM 5 % Chapter Four: Unpublished material not submitted for publication. Co-authored by Tim Dempster and Stephen E Swearer. LTB, TD and SES conceived and designed the experiment; LTB conducted the experiment and collected data with assistance from technical staff and volunteers; LTB analysed the data and wrote the manuscript; TD and SES provided editorial comments. Contributions: LTB 80 %, TD 10 %, SES 10 % Chapter Five: Unpublished material not submitted for publication. Co-authored by Stephen E Swearer, Tim Dempster. LTB, SES and TD conceived and designed the experiment; LTB conducted the experiment and collected data with assistance from technical staff and volunteers; LTB analysed the data and wrote the manuscript; SES and TD provided editorial comments. Contributions: LTB 80 %, SES 10 %, TD 10 % iii This research was funded by grants from the Holsworth Wildlife Research Endowment (Chapters Four and Five), the PADI Foundation (Chapter Five), the Victorian Environmental Assessment Council (Chapter Five), the Sustainable Aquaculture Lab – Temperate and Tropical (all chapters), the Research on the Ecology and Evolution (REEF) Lab (all chapters), and the Norwegian Seafood Research Fund (Chapter Three). All animal research was conducted in accordance with the animal ethics requirements of the University of Melbourne (Chapter Five: approval numbers 1413133 and 1413193) and Norwegian legislation on animal experimentation (Chapter Three: approval number 8264). Permits were obtained from the Victorian state government for collection and translocation of marine animals and algae for (Chapters Four and Five: RP919, RP1185, NP280, NP282). iv ACKNOWLEDGMENTS I would firstly like to thank my supervisors, Steve Swearer and Tim Dempster, for their unwavering support over the duration of my PhD. They have been everything I could have hoped for in a pair of supervisors. My friends and colleagues in the REEF and SALTT labs, past and present, provided helpful discussions and comments on my thesis chapters, and were universally great company to have a coffee or beer with, as were all my officemates in 131 and others around BioSciences 4. Special mentions go to Simon, Emily, Ben, Fran, Qike, Valeriya, Tyler, Matt, James, Jack, Ollie and Fletch for making me feel welcome in my first couple of years in Melbourne. Many people combined forces with me to get fieldwork done on the cold and murky waters of Port Phillip Bay. In alphabetical order: Dean Chamberlain, Seann Chia, Ben Cleveland, Emily Fobert, Molly Fredle, Akiva Gebler, Kevin Jensen, Valeriya Komyakova, Nina Kriegisch, Kevin Menzies, Rebecca Morris, Jack O’Connor, Simon Reeves, Juan Manuel Valero Rodriguez, Kyler Tan, Chris Taylor, João Teixiera, Oliver Thomas and Rod Watson (Victorian Marine Science Consortium). Apologies if I forgot anyone! Lance Wiffen provided access to his aquaculture leases at Clifton Springs and Grassy Point. John Ahern and Tania Long averted a couple of aquarium-related catastrophes in my absence, thanks and sorry! Thanks to my Norwegian collaborators and surrogate supervisors during my time there: Torstein Harboe, Ørjan Karlsen and Sonnich Meier. The work was made possible by numerous technical staff, researchers, expert cod fishermen and all-round nice people. I’d especially like to thank Margareth Møgster, Stig Ove Utskot, Theresa Aase, Michal Rejmer, Inger Semb Johansen, Nele Gunkel-Sauer, Kristine Hovland Holm, Yvonne Rong, Terje van der Meeren, Tord Skår, Velimir Nola and Glenn Sandtorv. I’d also like to thank the staff and students at Austevoll High School for taking us to Brandasund and back with a boatload of live cod. My family and friends back home in WA tolerated my long absence and my incommunicativeness during the busy times, and largely stayed away from the question “when will you be finished?”. Well played! Finally, but most importantly, I’d like to thank my partner Marina, who provided constant love and support, and made quite a few sacrifices to ensure that I had a clear run at this thesis. I hope it’s been worth it! v CONTENTS List of Tables ....................................................................................................................... ix List of Figures ....................................................................................................................... x Chapter One | General introduction General introduction ........................................................................................................... 1 References .......................................................................................................................... 9 Chapter Two | Impacts of marine and freshwater aquaculture on wildlife: a global meta- analysis Abstract ............................................................................................................................. 14
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