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Climate Change and Tropical Sponges

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Climate Change and Tropical Sponges CLIMATE CHANGE AND TROPICAL SPONGES: THE EFFECT OF ELEVATED pCO2 AND TEMPERATURE ON THE SPONGE HOLOBIONT HOLLY M. BENNETT A thesis submitted to the Victoria University of Wellington in fulfilment of the requirements for the degree of Doctor of Philosophy Victoria University of Wellington Te Whare Wānanga o te Ūpoko o te Ika a Māui 2017 Carteriospongia foliascens on the Great Barrier Reef, Australia. “I can mention many moments that were unforgettable and revelatory. But the most single revelatory three minutes was the first time I put on scuba gear and dived on a coral reef.” David Attenborough This thesis was conducted under the supervision of: Associate Professor James J. Bell (Primary supervisor) Victoria University of Wellington Wellington, New Zealand + Doctor Nicole S. Webster (Co-Supervisor) Australian Institute of Marine Science Townsville, Australia + Professor Simon K. Davy (Co-Supervisor) Victoria University of Wellington Wellington, New Zealand Abstract As atmospheric CO2 concentrations rise, associated ocean warming (OW) and ocean acidification (OA) are predicted to cause declines in reef-building corals globally, shifting reefs from coral-dominated systems to those dominated by less sensitive species. Sponges are important structural and functional components of coral reef ecosystems, but despite increasing field-based evidence that sponges may be ‘winners’ in response to environmental degradation, our understanding of how they respond to the combined effects of OW and OA is limited. This PhD thesis explores the response of four abundant Great Barrier Reef species – the phototrophic Carteriospongia foliascens and Cymbastela coralliophila and the heterotrophic Stylissa flabelliformis and Rhopaloeides odorabile to OW and OA levels predicted for 2100, under two CO2 Representative Concentration Pathways (RCPs). The overall aim of this research is to bridge gaps in our understanding of how these important coral reef organisms will respond to projected climate change, to begin to explore whether a sponge dominated state is a possible future trajectory for coral reefs. To determine the tolerance of adult sponges to climate change, these four species were exposed to OW and OA in the Australian Institute of Marine Science’s (AIMS) National Sea Simulator (SeaSim) in a 3-month experimental study. The first data chapter explores the physiological responses of these sponges to OW and OA to gain a broad understanding of sponge holobiont survival and functioning under these conditions. In this chapter I also address the hypothesis that phototrophic and heterotrophic sponges will exhibit differential responses to climate change. In the second and third data chapters I explore the cellular lipid and fatty acid composition of sponges, and how these biochemical constituents vary with OW and OA. Lipids and fatty acids are not only vital energy stores, they form the major components of cell membranes, and the structure and composition of these biochemical constituents ultimately determines the integrity and physiological competency of a cell. Therefore through these analyses I aimed to determine how OW and OA affects the metabolic balance of sponges, and to understand mechanisms underpinning observed systemic sponge responses. Finally, to provide greater insight into the population level impacts of climate change on tropical sponges, in the last data chapter I explore the response of the phototrophic species Carteriospongia foliascens to OW/OA throughout its developmental stages. 7 I found that while sponges can generally tolerate climate change scenarios predicted under the RCP6.0 conditions for 2100 (30ºC/ pH 7.8), environmental projections for the end of this century under the RCP8.5 (31.5ºC/ pH 7.6) will have significant implications for their survival. Temperature effects were much stronger than OA effects for all species; however, phototrophic and heterotrophic species responded differently to OA. Elevated pCO2 exacerbated temperature stress in heterotrophic sponges but somewhat ameliorated thermal stress in phototrophic species. Furthermore, sponges with siliceous spiculated skeletons resisted the RCP 8.5 conditions for longer than the aspiculate species. Biochemical analysis revealed that spiculated species also have greater cell membrane support features, which is likely to contribute to the observed stress tolerance. I also found that the additional energy available to phototrophic sponges under OA conditions may be used for investment into cell membrane support, providing protection against thermal stress. Finally, larval survival and settlement success of C. foliascens was unaffected by OW and OA treatments, and juvenile sponges exhibited greater tolerance than their adult counterparts, again with evidence that OA reduces OW stress for some of these life stages. Based on the species studied here, this thesis confirms that sponges are better able to deal with OW and OA levels predicted for 2100 under RCP6.0, compared to many corals for which survival in a high CO2 world requires OW to remain below 1.5°C. This suggests sponges may be future ‘winners’ on coral reefs under global climate change. However, if CO2 atm concentrations reach levels predicted under RCP8.5, the prognosis for sponge survival by the end of this century changes as inter-species sponge tolerances to OW and OA differ. Under this projection it is likely we will also start to see a shift in sponge populations to those dominated by phototrophic sponges with siliceous spiculated skeletons. Overall, this thesis gives a holistic view of OW and OA impacts on tropical sponges and provides the basis from which to explore the potential for a sponge-coral regime shift in a high CO2 world. 8 This thesis is dedicated to my grandparents; Hugh, Mary and Ana. 9 10 Acknowledgements First and foremost I would like to thank my supervisors, Associate Professor James Bell, Doctor Nicole Webster and Professor Simon Davy. Individually they are all inspiring as scientists, teachers and mentors; collectively an amazing supervisory team that I have been so privileged to learn from. I thank James for encouraging independence whilst providing unwavering guidance and support. I thank Nicole for being such a positive role-model, and for her endless support and motivation. I thank Simon for his support and commitment throughout my PhD. It was an absolute pleasure to work with all of them. During my PhD candidature I spent a significant amount of time at both Victoria University of Wellington (VUW) and the Australian Institute of Marine Science (AIMS). I owe a debt of gratitude to all of the people that I have worked with who have influenced and supported me along the way. Thank you to my peers, lab mates and friends from both VUW and AIMS, all of whom I have been so fortunate to share this journey with. In particular at VUW, the Bell lab group AKA “sponge club”, past and present; such a productive, supportive and fun group to be a part of. I hope our collaborations, field trips and after work drinks will continue into the future. I am also very grateful to the highly constructive AIMS sponge research team. I thank them for sharing their knowledge, providing feedback and advice and for maintaining such an open and positive work environment in which high calibre research flourishes. A significant proportion of my field, experimental and lab work was carried out at AIMS, and for that I have a number of people and teams I would like to thank. A huge thank you to the National Sea Simulator (SeaSim) team. I was so fortunate to carry out my experiments in SeaSim, and to have the support of such an incredibly competent group of people. Thank you to the marine operations guys and to the Fergusson crew for all of the epic field trips. A big thank you to the scientists, technicians, lab managers, receptionists, IT staff, security guards, cleaners and my commuter car companions at AIMS. From VUW I would like to specifically thank Daniel McNaughtan (Snout), and Stephen Journee for their dive support and training. Thank you also to Alan Hoverd for sharing his wisdom, and to all of the biological sciences personnel who have provided support along the way. I would now like to acknowledge those who have contributed to the individual chapters of my PhD thesis research. 11 Chapter two: I am incredibly grateful to all of the SeaSim staff involved in setting up the extensive experimental system for this work, and for their continued support whilst running the experiments. I am also thankful to Christine Altenrath and Sarah Sutfcliffe for their support in maintaining the experimental system and for sampling and processing tissue samples. I appreciate AIMS marine operations for facilitating collection trips, and Stephen Boyle and Philip Kearns for processing experimental water samples. I would like to acknowledge and thank a number of people who advised me on sampling methods, techniques and theory, in particular thank you to Florita Fores, Andrew Negri, Julia Strahl, Sam Noonan, Sven Uthicke, Heidi Luter, Manue Botte, Mari-Carmen Pineda, Emma Gibbon, Ken Ryan and Ross Hill. Thanks to Lisa Wood for her support with the data analysis. I acknowledge the four anonymous reviewers whose suggestions improved the published manuscript and the PADI foundation for providing funding that supported this research. I dedicate this chapter to Ivan Weiner (AIMS security guard) who passed in July 2014. Ivan was a reassuring presence and provider of company and food during the long nights that I spent working on experiments. Chapter’s two and three: I am extremely thankful for the support of Doctor David Francis. Dave taught me lipid extraction and analysis techniques; he processed all of the fatty acid samples and has worked closely with me in the interpretation and writing of these chapters, sharing his wisdom and re-directing me where necessary. I also wish to thank Jessica Conlan for sharing her expertise and Julia Strahl for supporting me in the lab. Chapter five: Thank you to Muhammad Abdul Wahab (Zuzu) from the Australian Institute of Marine Science for providing images, juvenile sponges, his time in the field and for passing on his knowledge of sponge reproduction and husbandry.
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