Recent research efforts have demonstrated increased bioerosion rates under experimentally elevated partial pressures of seawater carbon dioxide (pCO2 ) with or without increased temperatures, which may lead to net erosion on coral reefs in the future. However, this conclusion clearly depends on the ability of the investigated bioeroding organisms to survive and grow in the warmer and more acidic future environments, which remains unexplored. The excavating sponge Cliona orientalis Thiele, is a widely distributed bioeroding organism and symbiotic with dinoflagellates of the genus Symbiodinium. Using C. orientalis, an energy budget model was developed to calculate amounts of carbon directed into metabolic maintenance and growth. This model was tested under a range of CO2 emission scenarios (temperature + pCO2 ) appropriate to an Austral early summer. Under a pre-industrial scenario, present day (control) scenario, or B1 future scenario (associated with reducing the rate of CO2 emissions over the next few decades), C. orientalis maintained a positive energy budget, where metabolic demand was likely satisfied by autotrophic carbon provided by Symbiodinium and heterotrophic carbon via filter-feeding, suggesting sustainability. Under B1, C. orientalis likely benefited by a greater supply of photosynthetic products from its symbionts, which increased by up to 56% per unit area, and displayed an improved condition with up to 52% increased surplus carbon available for growth. Under an A1FI future scenario (associated with 'business-as-usual' CO2 emissions) bleached C. orientalis experienced the highest metabolic demand, but carbon acquired was insufficient to maintain the sponge, as indicated by a negative energy budget. These metabolic considerations suggest that previous observations of increased bioerosion under A1FI by C. orientalis may not last through the height of future A1FI summers, and survival of individual sponges may be dependent on the energy reserves (biomass) they have accumulated through the rest of the year.

Ocean acidification is a growing threat to coral growth and the accretion of coral reef ecosystems. Corals inhabiting environments that already endure extreme diel pCO 2 fluctuations, however, may represent acidification-resilient populations capable of persisting on future reefs. Here, we examined the impact of pCO 2 variability on the reef-building coral Pocillopora damicornis originating from reefs with contrasting environmental histories (variable reef flat versus stable reef slope) following reciprocal exposure to stable (218 ± 9) or variable (911 ± 31) diel pCO 2 amplitude (μtam) in aquaria over eight weeks. Endosymbiont density, photosynthesis and net calcification rates differed between origins but not treatment, whereas primary calcification (extension) was affected by both origin and acclimatization to novel pCO 2 conditions. At the cellular level, corals from the variable reef flat exhibited less intracellular pH (pHi) acidosis and faster pHi recovery rates in response to experimental acidification stress (pH 7.40) than corals originating from the stable reef slope, suggesting environmental memory gained from lifelong exposure to pCO 2 variability led to an improved ability to regulate acid–base homeostasis. These results highlight the role of cellular processes in maintaining acidification resilience and suggest that prior exposure to pCO 2 variability may promote more acidification-resilient coral populations in a changing climate.

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The bioeroding sponge Cliona orientalis is photosymbiotic with dinoflagellates of the genus Symbiodinium and is pervasive on the Great Barrier Reef. We investigated how C. orientalis responded to past and future ocean conditions in a simulated community setting. The experiment lasted over an Austral summer under four carbon dioxide emission scenarios: a pre-industrial scenario (PI), a present-day scenario (PD; control), and two future scenarios of combined ocean acidification and ocean warming, i.e., B1 (intermediate) and A1FI (extreme). The four scenarios also simulated natural variability of carbon dioxide partial pressure and temperature in seawater. Responses of C. orientalis generally remained similar between the PI and PD treatments. C. orientalis under B1 displayed a dramatic increase in lateral tissue extension, but bleached and displayed reduced rates of respiration and photosynthesis. Some B1 sponge replicates died by the end of the experiment. Under A1FI, strong bleaching and subsequent mortality of all C. orientalis replicates occurred at an early stage of the experiment. Mortality arrested bioerosion by C. orientalis under B1 and A1FI. Overall, the absolute amount of calcium carbonate eroded by C. orientalis under B1 or A1FI was similar to that under PI or PD at the end of the experiment. Although bioerosion rates were raised by short-term experimental acidification in previous studies, our findings from the photosymbiotic C. orientalis imply that the effects of bioerosion on reef carbonate budgets may only be temporary if the bioeroders cannot survive long-term in the future oceans.