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Bioeroding Sponges in a Time of Change

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Bioeroding Sponges in a Time of Change Bioeroding sponges in a time of change: insights into the physiology and cell biology of a photosymbiotic coral-eroding sponge Michelle Achlatis Master of Science; Bachelor of Science A thesis submitted for the degree of Doctor of Philosophy at The University of Queensland in 2018 School of Biological Sciences Abstract Anthropogenic climate change is altering the ecological balance of the world around us, and coral reefs are among the first ecosystems to reveal these fundamental changes. Consequently, there is an urgent need to understand how key services provided by reefs will change in the future. The ability of reefs to maintain positive carbonate balances despite their exposure to the erosive power of waves is fundamental to many services they provide. An important, but relatively unexplored facet of the carbonate balance of reefs, is their biological erosion by excavating sponges. Gaining greater insight into the physical drivers of this biological erosion, in addition to the potential responses of excavating sponges to future conditions is therefore the goal of this thesis. While healthy reefs maintain a positive budget, or at least equilibrium between construction and destruction of calcium carbonate (CaCO3), warming and ocean acidification have the potential to tip the scales towards net erosion. Excavating sponges, which are one of the major groups of CaCO3 bioeroders, belong to the perceived “winners” under future scenarios with their bioerosion rates expected to increase disproportionately. Despite the critical relevance of the effect of climate change on the excavating activity of bioeroding sponges, the physiological and metabolic processes that underpin the ecological success of such sponges on coral reefs are poorly understood. Some of the most competitive and destructive (to the CaCO3 framework) bioeroding sponges form a symbiosis with photosynthetic dinoflagellates of the genus Symbiodinium. The Great Barrier Reef sponge Cliona orientalis, used as a model in the current study, is an aggressive competitor that often overgrows and kills the calcareous corals that it erodes. A key question is: Is the vigour and competitive superiority of such sponges associated with the symbiosis they form with photosynthetic dinoflagellates? The role of dinoflagellates in host metabolism and host bioerosion capacity remains relatively unexplored. The first study in the present thesis attempts to shed light on the interaction between C. orientalis and its photosymbionts, while assessing the contribution of photosynthetic energy to the bioerosion activity (Chapter 2). The bioerosion rates of bleached (relatively free of symbionts), photosynthetically inactivated (treated with diuron) and control sponges were quantified in the light (day) and in the dark (night). These experiments show a clear relation between the holobiont photosynthetic activity and the day-time bioerosion capacity of the sponge. Night-time bioerosion was only partially explained by respiration rates and day-time photosynthetic activity that might lead to storage of photosynthetic outputs for night-time use. i The presence of a small prokaryotic community in the sponge, however, complicates the definitive attribution of all photosynthetic activity to Symbiodinium. There are multiple potential candidates for uptake of inorganic carbon (i.e. photosynthesis) or inorganic nitrogen within a clionaid holobiont, the latter potentially even carried out by the sponge itself. In a second study, isotopically enriched 13C-bicarbonate and 15N-ammonium were used to track the entry and distribution of inorganic carbon and nitrogen in the sponge holobiont (Chapter 3). Capitalizing on recent integration of isotopic labelling, transmission electron microscopy and nanoscale secondary ion mass spectrometry, isotopic enrichment of individual cell types and tissue structures of interest were visualized and quantified inside the outer photosynthetic layer of the sponge. This experiment unequivocally pinpointed Symbiodinium as the primary source of inorganic assimilation into organic material, illustrating that assimilated material is subsequently translocated to proximate sponge cells, in the absence of symbiont digestion. Finally, to assess the resilience of the symbiosis as well as the host’s dependence on Symbiodinium, the sponge holobiont was subjected to prolonged warming and acidification, under increased heterotrophic potential (Chapter 4). In a fully-crossed design that respects diurnal and seasonal fluctuations in seawater conditions, the sponges were exposed to independent and concomitant warming and acidification (projected as appropriate for a typical end of century, non-El Niño summer under “business-as-usual” carbon dioxide emissions), as well as diet supplementation with nitrogen-rich particulates. While acidification did not strongly affect erosion rates, diet supplementation accelerated them. Warming decelerated bioerosion rates and caused extensive bleaching and prevailing mortality of sponges, overriding the other factors and confirming a strong metabolic dependence of the sponge on its resident symbionts. This experiment indicates that the growth, bioerosion capacity and likelihood of survival of C. orientalis and similar photosymbiotic excavating sponges could be substantially reduced rather than increased on end-of-the-century reefs under “business-as-usual” emission profiles. In other words, although photosymbiotic excavating sponges benefit in many ways from their resident Symbiodinium, they are nonetheless vulnerable to prolonged heat stress, implying that they may not share the title of “winners” alongside their non- Symbiodinium-hosting counterparts on future coral reefs. ii Declaration by author This thesis is composed of my original work, and contains no material previously published or written by another person except where due reference has been made in the text. I have clearly stated the contribution by others to jointly-authored works that I have included in my thesis. I have clearly stated the contribution of others to my thesis as a whole, including statistical assistance, survey design, data analysis, significant technical procedures, professional editorial advice, financial support and any other original research work used or reported in my thesis. The content of my thesis is the result of work I have carried out since the commencement of my higher degree by research candidature and does not include a substantial part of work that has been submitted to qualify for the award of any other degree or diploma in any university or other tertiary institution. I have clearly stated which parts of my thesis, if any, have been submitted to qualify for another award. I acknowledge that an electronic copy of my thesis must be lodged with the University Library and, subject to the policy and procedures of The University of Queensland, the thesis be made available for research and study in accordance with the Copyright Act 1968 unless a period of embargo has been approved by the Dean of the Graduate School. I acknowledge that copyright of all material contained in my thesis resides with the copyright holder(s) of that material. Where appropriate I have obtained copyright permission from the copyright holder to reproduce material in this thesis and have sought permission from co-authors for any jointly authored works included in the thesis. iii Publications during candidature Peer-reviewed publications related to this thesis: Achlatis M, van der Zande RM, Schönberg CHL, Fang JKH, Hoegh-Guldberg O, Dove S. (2017). Sponge bioerosion on changing reefs: ocean warming poses physiological constraints to the success of a photosymbiotic excavating sponge. Sci Rep 7: 10705. Achlatis M, Pernice M, Green K, Guagliardo P, Kilburn MR, Hoegh-Guldberg O, Dove S. (2018). Single-cell measurement of ammonium and bicarbonate uptake within a photosymbiotic bioeroding sponge. ISME J 12: 1308–1318. Peer-reviewed publications not related to this thesis: Alexander BE, Achlatis M, Osinga R, van der Geest HG, Cleutjens JPM, Schutte B, de Goeij JM. (2015). Cell kinetics during regeneration in the sponge Halisarca caerulea: how local is the response to tissue damage? PeerJ 3: e820. Ramsby BD, Hill MS, Thornhill DJ, Steenhuizen SF, Achlatis M, Lewis AM, LaJeunesse TC. (2017). Sibling species of mutualistic Symbiodinium clade G from bioeroding sponges in the western Pacific and western Atlantic oceans. J Phycol 53: 951–960. Fang JKH, Schönberg CHL, Mello-Athayde MA, Achlatis M, Hoegh-Guldberg O, Dove S. (2018). Bleaching and mortality of a photosymbiotic bioeroding sponge under future carbon dioxide emission scenarios. Oecologia 187: 25-35. Brown KT, Bender-Champ D, Kubicek A, van der Zande R, Achlatis M, Hoegh-Guldberg O, Dove SG (2018). The dynamics of coral-algal interactions in space and time on the southern Great Barrier Reef. Front Mar Sci 5: 181. Hoegh-Guldberg O, Jacob D, Taylor M, Bindi M, Brown S, Camilloni I, Diedhiou A, Djalante R, et al. (2018). Chapter 3: Impacts of 1.5ºC global warming on natural and human systems. In: Global Warming of 1.5 °C, an IPCC special report on the impacts of global warming of 1.5 °C above pre- industrial levels. Intergovernmental Panel on Climate Change. (contributing author). iv Conference abstracts related to this thesis and presented by the candidate: “Future bioerosion on the Great Barrier Reef by the excavating sponge Cliona orientalis”, 89th Australian Coral Reef Society Conference, 2015, Daydream Island, Australia. “Putting the success
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