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Effects of Projected Near-Future Carbon Dioxide Levels on Cephalopod Physiology and Behaviour

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Effects of Projected Near-Future Carbon Dioxide Levels on Cephalopod Physiology and Behaviour ResearchOnline@JCU This file is part of the following work: Spady, Blake L. (2018) Effects of projected near-future carbon dioxide levels on cephalopod physiology and behaviour. PhD Thesis, James Cook University. Access to this file is available from: https://doi.org/10.25903/5d23f4bab9305 Copyright © 2018 Blake L. Spady. The author has certified to JCU that they have made a reasonable effort to gain permission and acknowledge the owners of any third party copyright material included in this document. If you believe that this is not the case, please email [email protected] Effects of projected near-future carbon dioxide levels on cephalopod physiology and behaviour Thesis submitted by: Blake L. Spady For the degree of Doctor of Philosophy College of Science and Engineering James Cook University October 2018 This thesis is dedicated to my father, Dennis Neal Spady. i Declaration of Ethics The research presented in this thesis was conducted in accordance with the JCU Animal Ethics Committee (A2189). Collection permits for study species were acquired from the Queensland Department of Agriculture, Fisheries and Forestry (170251). ii Statement on the Contribution of Others This thesis includes collaborative work with my advisors Dr. Sue-Ann Watson and Prof. Philip Munday. While undertaking these collaborations I was responsible for experimental design, animal collection and care, data collection, analysis, and interpretation of my results. My co- authors provided intellectual guidance, editorial assistance, statistical assistance, financial support, and technical assistance. Chapter 2 includes collaborations with Dr. Jodie Rummer and Tiffany Nay who contributed in experimental design and editorial assistance. Financial support was provided by the ARC Centre of Excellence for Coral Reef Studies (P. Munday and S-A. Watson), the PADI Foundation (B. Spady), the James Cook University Graduate Research Funding Scheme, and the College of Science and Engineering, James Cook University. James Cook University provided laboratory space and funding for technicians at the Marine and Aquaculture Research Facilities Unit. iii Acknowledgements I would like to first and most importantly thank my advisors, Sue-Ann Watson and Philip Munday, for putting in the effort to help me gain the most out of this experience. Sue-Ann, thank you for always being approachable and for your care not only for my work, but for my well-being; I always felt high up on your list of priorities. You have inspired me to always think carefully and critically, and to stay on the track towards my goals. Also, thanks for keeping me as your student even after I threw up on you in the field. Phil, you were never easy on me, and for that I will always be grateful. Knowing your expectations and aiming to surpass them has been the most constant source of motivation throughout my PhD. You have taught me how to stay sharp and have helped me develop my research skills in a way that nobody else could. I also have to thank you for ensuring that my wine glass was never empty. Infinite thanks to the technical staff at the Marine and Aquaculture Research Facilities Unit at James Cook University; Ben Lawes, Simon Wever, and Andrew Thompson. Aside from your incredible work, advice, and assistance, the daily coffee break with you guys is one of the things that kept me sane. I cannot express enough appreciation to Prof. Rhondda Jones for her statistical help and advice, which she was always so happy to provide. Thank you to all of my volunteers (Erin Weir, Selina Tang, and Sophie Stringer) for keeping those bag filters clean and never complaining. Many thanks to Jenni Donelson for her never ending (and I mean NEVER ending!) advice on anything and everything. You’re a well of knowledge and I appreciate your generosity in sharing it with me. Shannon McMahon, thanks for always being available for help whether it be finding something in the lab, lifting a Reln, or occasionally even something that actually has to do with science. Your patience and calm approach to problems has given me more personal insight than you realise. Michael Jarrold, thanks for always being fun and in good spirits. I’m sure you gave me some good advice in the past too, but I could never understand what you were saying. Rachel Spinks, thanks for always talking through things with me (and not just stats!), you are one of the most kind-hearted people I know. Thanks to Taryn Laubenstein for being there to whinge with me about why doing lab experiments with live iv animals was a terrible life decision. Thanks to my former officemates and life-long friends, Meg Welch and Donny Warren. Meg, you have always been there when I needed someone to talk to and have been one of my strongest support beams since I started research. Donny, sharing an office with you was a hell of a lot of fun…I’m glad you left though because I probably wouldn’t be finished with this thesis if you had stayed. I’d also like to thank my friends outside of my lab group. My boatin’ buddy, Eva McClure…thanks for everything, really. You are an incredible and selfless friend and you owe me a burrito. Tory Chase, thanks for always trying to get me away from my PhD to have fun; chatting with you three mornings per week (most weeks) has kept my spirits up. Everyone needs a friend like you. Margaux Hein and Athena Andreosso, you two are the first long- lasting friendships that I made in this country. I don’t think I would have lasted long here were it not for a friendship like yours in the early days. Local Lewie McMurran, what can I say that isn’t already known. Other honourable mentions: Katie Motson, Bert Strite, Laura Richardson, Bjorn Illing, Dani Nembhard, and Bridie Allan Gibbs. I have nice things to say about you all too, but I’m running out of space! Finally, thank you to my family. Mom, thanks so much for hanging in there while I moved to the other side of the world to do this. Your constant support and very frequent text messages mean the world to me. Brock, you have always been someone I have looked up to and I hope I’ve made you proud. Maud, you’ve been the most amazing companion throughout this PhD. Thank you so much for loving and supporting me even when I’ve been no fun and spent more time with my squid than with you. You have been the best part of this PhD. I can’t wait for our adventures in the years to come. v General Abstract Oceanic uptake of anthropogenic carbon dioxide (CO2) is causing changes to seawater chemistry, a process known as ocean acidification. This has the potential to negatively affect a wide variety of marine organisms. To date, most studies into the effects of elevated CO2 on marine organisms have focused on highly calcified invertebrates and fishes, with a variety of effects observed, including impacts on early life history development, respiration, behaviour, and learning. Despite their importance in marine ecosystems, comparatively little is known about the possible effects of rising CO2 levels on cephalopods. In this thesis, I investigate the effects of CO2 levels projected for the end of this century on the aerobic scope, reproduction, development, predatory behaviours, and learning in two species of tropical cephalopod from different taxonomic orders, the two-toned pygmy squid (Idiosepius pygmaeus) and the bigfin reef squid (Sepioteuthis lessoniana). In Chapter 2, I investigate the effects of elevated CO2 on the minimum and maximum oxygen uptake rates, and aerobic scope of both I. pygmaeus and S. lessoniana. Due to the pH sensitive oxygen transport of cephalopods, I expected adverse effects on oxygen uptake rates. However, there were no effects of elevated CO2 exposure on oxygen uptake rates or aerobic scope. This suggests a level of tolerance to elevated CO2 in both species. The ability of these two cephalopod species to cope with long-term exposure to elevated CO2 without detriment to their aerobic scope suggests that the energy available to partition to other important tasks, such as reproduction and growth, may remain optimal at elevated CO2. One of the more commonly observed effects of elevated CO2 on marine molluscs is altered reproduction and early life history development. In Chapter 3, I test the effects of elevated CO2 on reproduction and the potential for effects after parental exposure on early development in I. pygmaeus. Despite the lack of effects of elevated CO2 on the aerobic scope of adults observed in Chapter 2, there were adverse effects of elevated CO2 on reproduction and development. Parents held at elevated CO2 produced clutches with 40% fewer eggs compared with parents in ambient control conditions. Embryo area, measured directly after spawning, was significantly reduced in the elevated CO2 treatment compared to controls, and remained smaller throughout development. There was no effect of elevated CO2 on fertility, time to hatch, or hatching success. Lastly, female squid laid eggs >40% closer together at elevated CO2 compared with the controls, indicating a possible effect of elevated CO2 on egg- vi laying behaviour. The negative effects observed here appear to be predominately a response to parental exposure to elevated CO2 rather than exposure of the eggs themselves. As the potential for adaptation is strongly influenced by reproductive success, these effects could have consequences to the capacity of I. pygmaeus to cope with future ocean conditions. In Chapter 4, I investigate the effects of elevated CO2 on the predatory behaviours of both I. pygmaeus and S. lessoniana. Both species exhibited an increased latency to attack prey and displayed altered body pattern choice during the attack sequence at elevated CO2.
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