Marine heatwaves modulate the genotypic and physiological responses of reef-building corals to subsequent heat stress.

Back-to-back marine heatwaves in 2016 and 2017 resulted in severe coral bleaching and mortality across the Great Barrier Reef (GBR). Encouragingly, some corals that survived these events exhibit increased bleaching resistance and may represent thermally tolerant populations that can better cope with ocean warming. Using the GBR as a natural laboratory, we investigated whether a history of minimal (Heron Island) or severe (Lizard Island) coral bleaching in 2016 and 2017 equates to stress tolerance in a successive heatwave (2020). We examined the genetic diversity, physiological performance, and trophic plasticity of juvenile (<10 cm) and adult (>25 cm) corals of two common genera (Pocillopora and Stylophora). Despite enduring greater cumulative heat stress (6.3°C week-1 vs. 5.6°C week-1), corals that experienced the third marine heatwave in 5 years (Lizard) exhibited twice as high survival and visual bleaching thresholds compared to corals that had not experienced significant bleaching in >10 years (Heron). Surprisingly, only one shared host-Symbiodiniaceae association was uncovered between locations (Stylophora pistillata-Cladocopium "C8 group") and there was no genetic overlap in Pocillopora-Cladocopium partnerships, suggesting turnover in species composition from recent marine heatwaves. Corals within the species complex Pocillopora that survived the 2016 and 2017 marine heatwaves at Lizard Island were the most resilient, exhibiting three times greater calcification rates than conspecifics at Heron Island. Further, surviving corals (Lizard) had distinct isotopic niches, lower host carbon, and greater host protein, while conspecifics that had not experienced recent bleaching (Heron) had two times greater symbiont carbon content, suggesting divergent trophic strategies that influenced survival (i.e., greater reliance on heterotrophy vs. symbiont autotrophy, respectively). Ultimately, while corals may experience less bleaching and survive repeated thermal stress events, species-specific trade-offs do occur, leaving open many questions related to the long-term health and recovery of coral reef ecosystems in the face of intensifying marine heatwaves.

Environmental memory gained from exposure to extreme pCO2 variability promotes coral cellular acid-base homeostasis.

Ocean acidification is a growing threat to coral growth and the accretion of coral reef ecosystems. Corals inhabiting environments that already endure extreme diel pCO2 fluctuations, however, may represent acidification-resilient populations capable of persisting on future reefs. Here, we examined the impact of pCO2 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 pCO2 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 pCO2 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 pCO2 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 pCO2 variability may promote more acidification-resilient coral populations in a changing climate.

Colonies of Acropora formosa with greater survival potential have reduced calcification rates.

Coral reefs are facing increasingly devasting impacts from ocean warming and acidification due to anthropogenic climate change. In addition to reducing greenhouse gas emissions, potential solutions have focused either on reducing light stress during heating, or on the potential for identifying or engineering "super corals". A large subset of these studies, however, have tended to focus primarily on the bleaching response of corals, and assume erroneously that corals that bleach earlier in a thermal event die first. Here, we explore how survival, observable bleaching, coral skeletal growth (as branch extension and densification), and coral tissue growth (protein and lipid concentrations) varies for conspecifics collected from distinctive reef zones at Heron Island on the Southern Great Barrier Reef. A reciprocal transplantation experiment was undertaken using the dominant reef building coral (Acropora formosa) between the highly variable reef flat and the less variable reef slope environments. Coral colonies originating from the reef flat had higher rates of survival and amassed greater protein densities but calcified at reduced rates compared to conspecifics originating from the reef slope. The energetics of both populations however potentially benefited from greater light intensity present in the shallows. Reef flat origin corals moved to the lower light intensity of the reef slope reduced protein density and calcification rates. For A. formosa, genetic differences, or long-term entrainment to a highly variable environment, appeared to promote coral survival at the expense of calcification. The response decouples coral survival from carbonate coral reef resilience, a response that was further exacerbated by reductions in irradiance. As we begin to discuss interventions necessitated by the CO2 that has already been released into the atmosphere, we need to prioritise our focus on the properties that maintain valuable carbonate ecosystems. Rapid and dense calcification by corals such as branching Acropora is essential to the ability of carbonate coral reefs to rebound following disturbance events and maintain 3D structure but may be the first property that is sacrificed to enable coral genet survival under stress.

Differential impact of heat stress on reef-building corals under different light conditions.

Heat stress is an environmental factor that regularly challenges the well-being of living organisms. This study aims to examine the physiological changes happening in two reef-building coral species exposed to thermal stress under various light conditions. The two ecologically relevant heatwave scenarios were applied under ambient lights (high irradiance) and reduced light conditions (250 and < 10 µmol photons m-2 s-1). Corals were exposed to elevated temperatures of 32°C (plus 6°) for a period of 1 up to 5 days corresponding to heatwaves reported on the Great Barrier Reef (GBR) that were associated with coral bleaching. We monitored changes in the physiological performance of these two coral species by measuring symbionts and corals' physiological parameters including symbiont density, levels of multiple algal pigments (chlorophyll a and peridinin), as well as the changes in the host protein concentration. During the short-term heat stress, both species were with stable physiological performance with the only exception of Stylophora pistillata under ambient lights. These results show that S. pistillata was negatively influenced by a synergistic effect of temperature and high irradiance resulting in the first signs of bleaching after only 24h of thermal stress. Exposure to prolonged thermal stress, characterised with a slower rate of temperature increase, affected both coral species investigated and resulted in bleaching mainly by day 5. Interestingly, severe light reduction (<10 µmol photons m-2 s-1) made Acropora millepora corals more thermally sensitive and resulted in earlier signs of bleaching (on day 3). These findings indicate that there was a synergistic effect of very low lights and thermal stress that caused higher levels of bleaching in A. millepora. Our results revealed differential thermal sensitivity for two branching corals exposed to different thermal stress scenarios under various light irradiance conditions, naturally found in their existing habitats. Consequently, global warming may have a differential impact on coral reef biodiversity depending on light availability.

Bleaching and mortality of a photosymbiotic bioeroding sponge under future carbon dioxide emission scenarios.

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.

Effects of ocean warming and acidification on the energy budget of an excavating sponge.

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.

Sponge biomass and bioerosion rates increase under ocean warming and acidification.

The combination of ocean warming and acidification as a result of increasing atmospheric carbon dioxide (CO2 ) is considered to be a significant threat to calcifying organisms and their activities on coral reefs. How these global changes impact the important roles of decalcifying organisms (bioeroders) in the regulation of carbonate budgets, however, is less understood. To address this important question, the effects of a range of past, present and future CO2 emission scenarios (temperature + acidification) on the excavating sponge Cliona orientalis Thiele, 1900 were explored over 12 weeks in early summer on the southern Great Barrier Reef. C. orientalis is a widely distributed bioeroder on many reefs, and hosts symbiotic dinoflagellates of the genus Symbiodinium. Our results showed that biomass production and bioerosion rates of C. orientalis were similar under a pre-industrial scenario and a present day (control) scenario. Symbiodinium population density in the sponge tissue was the highest under the pre-industrial scenario, and decreased towards the two future scenarios with sponge replicates under the 'business-as-usual' CO2 emission scenario exhibiting strong bleaching. Despite these changes, biomass production and the ability of the sponge to erode coral carbonate materials both increased under the future scenarios. Our study suggests that C. orientalis will likely grow faster and have higher bioerosion rates in a high CO2 future than at present, even with significant bleaching. Assuming that our findings hold for excavating sponges in general, increased sponge biomass coupled with accelerated bioerosion may push coral reefs towards net erosion and negative carbonate budgets in the future.