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The worldwide decline of coral reefs has renewed interest in coral communities at the edge of environmental limits because they have the potential to serve as resilience hotspots and climate change refugia, and can provide insights into how coral reefs might function in future ocean conditions. These coral communities are often referred to as marginal or extreme but few definitions exist and usage of these terms has therefore been inconsistent. This creates significant challenges for categorising these often poorly studied communities and synthesising data across locations. Furthermore, this impedes our understanding of how coral communities can persist at the edge of their environmental limits and the lessons they provide for future coral reef survival. Here, we propose that marginal and extreme coral communities are related but distinct and provide a novel conceptual framework to redefine them. Specifically, we define coral reef extremeness solely based on environmental conditions (i.e., large deviations from optimal conditions in terms of mean and/or variance) and marginality solely based on ecological criteria (i.e., altered community composition and/or ecosystem functioning). This joint but independent assessment of environmental and ecological criteria is critical to avoid common pitfalls where coral communities existing outside the presumed optimal conditions for coral reef development are automatically considered inferior to coral reefs in more traditional settings. We further evaluate the differential potential of marginal and extreme coral communities to serve as natural laboratories, resilience hotspots and climate change refugia, and discuss strategies for their conservation and management as well as priorities for future research. Our new classification framework provides an important tool to improve our understanding of how corals can persist at the edge of their environmental limits and how we can leverage this knowledge to optimise strategies for coral reef conservation, restoration and management in a rapidly changing ocean.

Split-plot experimental data are often analyzed as if the data came from a completely randomized design. As is well known, ignoring the different levels of randomization and replication can lead to serious inferential errors. However, in some experiments, including many of the ocean global change experiments that motivated this research, variation between whole-plot experimental units may be small relative to variation between subplot units. Even though a factorial analysis will often perform poorly in general, in this special case it outperforms a split-plot analysis, providing narrower confidence intervals for treatment means and differences with coverage rates close to the desired level. The performance of the proposed model-averaged analysis was compared to a classical split-plot analysis via a simulation study, and its utility demonstrated for an ocean global change experiment examining growth and condition of a juvenile mussel species. In our simulation study, model-averaged confidence intervals for whole-plot treatment means or comparisons of means were up to 40% narrower than split-plot confidence intervals while maintaining close to nominal coverage rates. In our example experiment, we observed narrowing of up to 25%. We recommend model averaging as a preferred approach when variation between whole-plot experimental units is expected to be less than between subplot units, with a few caveats for studies with very few replicates.

Coralline algae perform important ecological roles in nearshore marine ecosystems globally by promoting the settlement of invertebrate larvae and enhancing biodiversity by creating habitat. However, these roles are severely threatened by global environmental changes. Most coralline algae are extremely difficult to identify, and DNA sequencing has revealed rampant inaccuracy of morpho-anatomical approaches to distinguish species, and even genera. If appropriate identification methods are not reported, or even used, we will be left with an uninterpretable body of literature where the species-specific biology of coralline algae cannot be validated. This will make it difficult to determine the impact a changing ocean may have on these ecologically important species. We reveal the magnitude of the issue in coralline algal research—both the identification methods used and the reporting of identification protocols. An analysis of 341 articles over the past decade revealed that only 7.6% used molecular methods, with over 70% not reporting any details of how species were identified. While many coralline algal taxonomists understand that the majority of species cannot be identified morphologically, this message has not disseminated to the ecological and physiological community. We provide a series of guidelines for conducting DNA-based identifications and strongly recommend the use of these methods over less informative morpho-anatomical techniques. Most importantly, the methods of identification should be adequately reported. Without following these guidelines, research on coralline algae runs the risk of collecting uninterpretable data, and conducting irreproducible science, slowing our ability to determine how these important species will respond to future ocean conditions.

Coral reefs are iconic ecosystems with immense ecological, economic and cultural value, but globally their carbonate-based skeletal construction is threatened by ocean acidification (OA). Identifying coral species that have specialised mechanisms to maintain high rates of calcification in the face of declining seawater pH is of paramount importance in predicting future species composition, and growth of coral reefs. Here, we studied multiple coral species from two distinct volcanic CO2 seeps in Papua New Guinea to assess their capacity to control their calcifying fluid (CF) chemistry. Several coral species living under conditions of low mean seawater pH, but with either low or high variability in seawater pH, were examined and compared with those living in ‘normal’ (non-seep) ambient seawater pH. We show that when mean seawater pH is low but highly variable, corals have a greater ability to maintain constant pHcf in their CF, but this characteristic was not linked with changes in abundance. Within less variable low pH seawater, corals with limited reductions in pHcf at the seep sites compared with controls tended to be more abundant at the seep site than at the control site. However, this finding was strongly influenced by a single species (Montipora foliosa), which was able to maintain complete pHcf homeostasis. Overall, although our findings indicate that there might be an association between ecological success and greater pHcf homeostasis, further research with additional species and at more sites with differing seawater pH regimes is required to solidify inferences regarding coral ecological success under future OA.

Coralline algae are an essential element of benthic ecosystems throughout the ocean’s photic zone. Yet, the role of light in shaping the physiology of coralline algae from cold-water, low-light habitats is poorly understood. Here, we assess the calcification physiology of five cool-temperate coralline algae in response to different irradiances over three months. We show that in contrast to current models focused on warmer water species, previously observed enhancement of calcification rates by photosynthesis is largely limited to lower irradiances, and that the removal of CO2 from the calcifying fluid (CF) is not the underlying mechanism of this enhancement. Instead, this likely occurs via two processes: 1) increased ion pumping rates to elevate the calcium carbonate saturation state in the CF; and 2) a higher daytime pH in the diffusion boundary layer that raises pHCF. However, as irradiance increases, ion pumping becomes increasingly saturated limiting further enhancements. Our results also suggest the existence of two calcification strategies in coralline algae and indicate that magnesium incorporation is determined by the internal magnesium to calcium ratio [Mg]CF/[Ca]CF. This study adds to our mechanistic understanding of calcification in coralline and fills in much needed knowledge about the role of light in controlling their physiology.

Ocean warming (OW) and acidification (OA) are two of the greatest global threats to the persistence of coral reefs. Calcifying reef taxa such as corals and coralline algae provide the essential substrate and habitat in tropical reefs but are at particular risk due to their susceptibility to both OW and OA. OW poses the greater threat to future reef growth and function, via its capacity to destabilise the productivity of both taxa, and to cause mass bleaching events and mortality of corals. Marine heatwaves are projected to increase in frequency, intensity, and duration over the coming decades, raising the question of whether coral reefs will be able to persist as functioning ecosystems and in what form. OA should not be overlooked, as its negative impacts on the calcification of reef-building corals and coralline algae will have consequences for global reef accretion. Given that OA can have negative impacts on the reproduction and early life stages of both coralline algae and corals, the interdependence of these taxa may result in negative feedbacks for reef replenishment. However, there is little evidence that OA causes coral bleaching or exacerbates the effects of OW on coral bleaching. Instead, there is some evidence that OA alters the photo-physiology of both taxa. Tropical coralline algal possess shorter generation times than corals, which could enable more rapid evolutionary responses. Future reefs will be dominated by taxa with shorter generation times and high plasticity, or those individuals inherently resistant and resilient to both marine heatwaves and OA.

Coral reefs are iconic ecosystems with immense ecological, economic and cultural value, but globally their carbonate-based skeletal construction is threatened by ocean acidification (OA). Identifying coral species that have specialised mechanisms to maintain high rates of calcification in the face of declining seawater pH is of paramount importance in predicting future species composition, and growth of coral reefs. Here, we studied multiple coral species from two distinct volcanic CO

Ocean warming (OW) and marine heatwaves (MHWs) rapidly transform marine ecosystems, especially when they impact keystone or foundation species. Foundation species such as kelps, fucoids and corals are highly sensitive to heat stress, which threatens the future of temperate seaweed forests and tropical reefs. However, functioning and resilience of these systems also relies on the less conspicuous coralline algae, whose thermal tolerances have gone largely untested. Here, we examined the sensitivity of four temperate coralline algal morphotypes from three different species to four realistic present day and future OW and MHW scenarios (ambient [16°C constant]; ambient+MHW [16°C baseline + a symmetric two-week heatwave with a peak intensity of 18.7°C]; future [18.7°C constant]; future+MHW [18.7°C baseline + a symmetric two-week heatwave with a peak intensity of 21.4°C]). Photo-physiology (e.g., Fv/Fm) and calcification physiology (e.g., proxies for calcifying fluid saturation state ΩCF) were generally unaffected by the treatments, implying a high thermo-tolerance of our study species compared to other important marine foundation species. We ascribe this mainly to their photosynthetic apparatus that, unlike in other photoautotrophs, continued to function under heat stress. Experimental evidence presented here and elsewhere implies that coralline algae are likely to continue to play their crucial ecological roles in a warming ocean. Yet, such predictions are fraught with uncertainty due to the substantial gaps in our knowledge. We attempt to highlight some of these gaps and aim to present potential physiological underpinnings of their thermo-tolerance.

Ocean acidification (OA) is a major threat to the persistence of biogenic reefs throughout the world's ocean. Coralline algae are comprised of high magnesium calcite and have long been considered one of the most susceptible taxa to the negative impacts of OA. We summarize these impacts and explore the causes of variability in coralline algal responses using a review/qualitative assessment of all relevant literature, meta-analysis, quantitative assessment of critical responses, and a discussion of physiological mechanisms and directions for future research. We find that most coralline algae experienced reduced abundance, calcification rates, recruitment rates, and declines in pH within the site of calcification in laboratory experiments simulating OA or at naturally elevated CO2 sites. There were no other consistent physiological responses of coralline algae to simulated OA (e.g., photo-physiology, mineralogy, and survival). Calcification/growth was the most frequently measured parameters in coralline algal OA research, and our meta-analyses revealed greater declines in seawater pH were associated with significant decreases in calcification in adults and similar but nonsignificant trends for juveniles. Adults from the family Mesophyllumaceae also tended to be more robust to OA, though there was insufficient data to test similar trends for juveniles. OA was the dominant driver in the majority of laboratory experiments where other local or global drivers were assessed. The interaction between OA and any other single driver was often additive, though factors that changed pH at the surface of coralline algae (light, water motion, epiphytes) acted antagonistically or synergistically with OA more than any other drivers. With advances in experimental design and methodological techniques, we now understand that the physiology of coralline algal calcification largely dictates their responses to OA. However, significant challenges still remain, including improving the geographic and life-history spread of research effort and a need for holistic assessments of physiology.

Ocean acidification (OA) is a major threat to coral reefs, which are built by calcareous species. However, long-term assessments of the impacts of OA are scarce, limiting the understanding of the capacity of corals and coralline algae to acclimatize to high partial pressure of carbon dioxide ( $${p}_{\mathrm{CO}_{2}}$$ ) levels. Species-specific sensitivities to OA are influenced by its impacts on chemistry within the calcifying fluid (CF). Here, we investigate the capacity of multiple coral and calcifying macroalgal species to acclimatize to elevated $${p}_{\mathrm{CO}_{2}}$$ by determining their chemistry in the CF during a year-long experiment. We found no evidence of acclimatization to elevated $${p}_{\mathrm{CO}_{2}}$$ across any of the tested taxa. The effects of increasing seawater $${p}_{\mathrm{CO}_{2}}$$ on the CF chemistry were rapid and persisted until the end of the experiment. Our results show that acclimatization of the CF chemistry does not occur within one year, which confirms the threat of OA for future reef accretion and ecological function. Calcifying marine species are threatened by ocean acidification. A year-long study of calcifying fluid chemistry shows that reef species, both corals and calcifying macroalgal species, were not able to adapt to ocean acidification.

The future of coral reef ecosystems is under threat because vital reef-accreting species such as coralline algae are highly susceptible to ocean acidification. Although ocean acidification is known to reduce coralline algal growth rates, its direct effects on the development of coralline algal reproductive structures (conceptacles) is largely unknown. Furthermore, the long-term, multi-generational response of coralline algae to ocean acidification is extremely understudied. Here, we investigate how mean pH, pH variability and the pH regime experienced in their natural habitat affect coralline algal conceptacle abundance and size across six generations of exposure. We show that second-generation coralline algae exposed to ocean acidification treatments had conceptacle abundances 60% lower than those kept in present-day conditions, suggesting that conceptacle development is initially highly sensitive to ocean acidification. However, this negative effect of ocean acidification on conceptacle abundance disappears after three generations of exposure. Moreover, we show that this transgenerational acclimation of conceptacle development is not facilitated by a trade-off with reduced investment in growth, as higher conceptacle abundances are associated with crusts with faster growth rates. These results indicate that the potential reproductive output of coralline algae may be sustained under future ocean acidification.

Significance The growth of coral reefs is threatened by the dual stressors of ocean warming and acidification. Despite a wealth of studies assessing the impacts of climate change on individual taxa, projections of their impacts on coral reef net carbonate production are limited. By projecting impacts across 233 different locations, we demonstrate that the majority of coral reefs will be unable to maintain positive net carbonate production globally by the year 2100 under representative concentration pathways RCP4.5 and 8.5, while even under RCP2.6, coral reefs will suffer reduced accretion rates. Our results provide quantitative projections of how different climate change stressors will influence whole ecosystem carbonate production across coral reefs in all major ocean basins., Ocean warming and acidification threaten the future growth of coral reefs. This is because the calcifying coral reef taxa that construct the calcium carbonate frameworks and cement the reef together are highly sensitive to ocean warming and acidification. However, the global-scale effects of ocean warming and acidification on rates of coral reef net carbonate production remain poorly constrained despite a wealth of studies assessing their effects on the calcification of individual organisms. Here, we present global estimates of projected future changes in coral reef net carbonate production under ocean warming and acidification. We apply a meta-analysis of responses of coral reef taxa calcification and bioerosion rates to predicted changes in coral cover driven by climate change to estimate the net carbonate production rates of 183 reefs worldwide by 2050 and 2100. We forecast mean global reef net carbonate production under representative concentration pathways (RCP) 2.6, 4.5, and 8.5 will decline by 76, 149, and 156%, respectively, by 2100. While 63% of reefs are projected to continue to accrete by 2100 under RCP2.6, 94% will be eroding by 2050 under RCP8.5, and no reefs will continue to accrete at rates matching projected sea level rise under RCP4.5 or 8.5 by 2100. Projected reduced coral cover due to bleaching events predominately drives these declines rather than the direct physiological impacts of ocean warming and acidification on calcification or bioerosion. Presently degraded reefs were also more sensitive in our analysis. These findings highlight the low likelihood that the world’s coral reefs will maintain their functional roles without near-term stabilization of atmospheric CO2 emissions.

Coral reefs provide critical ecological and geomorphic (e.g. sediment production for reef-fronted shoreline maintenance) services, which interact in complex and dynamic ways. These services are under threat from climate change, requiring dynamic modelling approaches that predict how reef systems will respond to different future climate scenarios. Carbonate budgets, which estimate net reef calcium carbonate production, provide a comprehensive ‘snap-shot’ assessment of reef accretionary potential and reef stability. These budgets, however, were not intended to account for the full suite of processes that maintain coral reef services or to provide predictive capacity on longer timescales (decadal to centennial). To respond to the dual challenges of enhancing carbonate budget assessments and advancing their predictive capacity, we applied a novel model elicitation and review method to create a qualitative geo-ecological carbonate reef system model that links geomorphic, ecological and physical processes. Our approach conceptualizes relationships between net carbonate production, sediment transport and landform stability, and rates knowledge confidence to reveal major knowledge gaps and critical future research pathways. The model provides a blueprint for future coral reef research that aims to quantify net carbonate production and sediment dynamics, improving our capacity to predict responses of reefs and reef-fronted shorelines to future climate change.

Ocean warming, ocean acidification and overfishing are major threats to the structure and function of marine ecosystems. Driven by increasing anthropogenic emissions of CO2, ocean warming is leading to global redistribution of marine biota and altered ecosystem dynamics, while ocean acidification threatens the ability of calcifying marine organisms to form skeletons due to decline in saturation state of carbonate Ω and pH. In Tasmania, the interaction between overfishing of sea urchin predators and rapid ocean warming has caused a phase-shift from productive kelp beds to overgrazed sea urchin barren grounds, however potential impacts of ocean acidification on this system have not been considered despite this threat for marine ecosystems globally. Here we use automated loggers and point measures of pH, spanning kelp beds and barren grounds, to reveal that kelp beds have the capacity to locally ameliorate effects of ocean acidification, via photosynthetic drawdown of CO2, compared to unvegetated barren grounds. Based on meta-analysis of anticipated declines in physiological performance of grazing urchins to decreasing pH and assumptions of nil adaptation, future projection of OA across kelp-barrens transition zones reveals that kelp beds could act as important pH refugia, with urchins potentially becoming increasingly challenged at distances >40 m from kelp beds. Using spatially explicit simulation of physicochemical feedbacks between grazing urchins and their kelp prey, we show a stable mosaicked expression of kelp patches to emerge on barren grounds. Depending on the adaptative capacity of sea urchins, future declines in pH appear poised to further alter phase-shift dynamics for reef communities; thus, assessing change in spatial-patterning of reef-scapes may indicate cascading ecological impacts of ocean acidification.

Crustose coralline algae play a crucial role in the building of reefs in the photic zones of nearshore ecosystems globally, and are highly susceptible to ocean acidification1–3. Nevertheless, the extent to which ecologically important crustose coralline algae can gain tolerance to ocean acidification over multiple generations of exposure is unknown. We show that, while calcification of juvenile crustose coralline algae is initially highly sensitive to ocean acidification, after six generations of exposure the effects of ocean acidification disappear. A reciprocal transplant experiment conducted on the seventh generation, where half of all replicates were interchanged across treatments, confirmed that they had acquired tolerance to low pH and not simply to laboratory conditions. Neither exposure to greater pH variability, nor chemical conditions within the micro-scale calcifying fluid internally, appeared to play a role in fostering this capacity. Our results demonstrate that reef-accreting taxa can gain tolerance to ocean acidification over multiple generations of exposure, suggesting that some of these cosmopolitan species could maintain their critical ecological role in reef formation. Crustose coralline algae help build coral reef structures through calcification, a process threatened under ocean acidification. Juvenile algae were highly sensitive on initial exposure to ocean acidification, but continued exposure over six generations showed a gain of tolerance.

Reef-building corals are surrounded by complex microenvironments (i.e. concentration boundary layers) that partially isolate them from the ambient seawater. Although the presence of such concentration boundary layers (CBLs) could potentially play a role in mitigating the negative impacts of climate change stressors, their role is poorly understood. Furthermore, it is largely unknown how heat stress-induced bleaching affects O2 and pH dynamics across the CBLs of coral, particularly in branching species. We experimentally exposed the common coral species Acropora aspera to heat stress for 13 d and conducted a range of physiological and daytime microsensor measurements to determine the effects of bleaching on O2 and pH gradients across the CBL. Heat stress equivalent to 24 degree heating days (3.4 degree heating weeks) resulted in visible bleaching and significant declines in photochemical efficiency, photosynthesis rates and photosynthesis to respiration (P/R) ratios, whereas dark respiration and calcification rates were not impacted. As a consequence, bleached A. aspera had significantly lower (− 13%) surface O2 concentrations during the day than healthy corals, with concentrations being lower than that of the ambient seawater, thus resulting in O2 uptake from the seawater. Furthermore, we show here that Acropora, and potentially branching corals in general, have among the lowest surface pH elevation of all corals studied to date (0.041 units), which could contribute to their higher sensitivity to ocean acidification. Additionally, bleached A. aspera no longer elevated their surface pH above ambient seawater values and, therefore, had essentially no [H+] CBL. These findings demonstrate that heat stress-induced bleaching has negative effects on pH elevation and [H+] CBL thickness, which may increase the overall susceptibility of coral to the combined impacts of ocean acidification and warming.

The threat posed by ocean acidification (OA) to the diversity and productivity of New Zealand marine ecosystems is assessed in a synthesis of published trends and impacts. A 20-year time series in Subantarctic water, and a national coastal monitoring programme, provide insight into pH variability, and context for experimental design, modelling and projections. A review of the potential impact of changes in the carbonate system on the major phyla in New Zealand waters confirms international observations that calcifying organisms, and particularly their early life-history stages, are vulnerable. The synthesis considers ecosystem and socio-economic impacts, and identifies current knowledge gaps and future research directions, including mechanistic studies of OA sensitivity. Advanced ecosystem models of OA, that incorporate the indirect effects of OA and interactions with other climate stressors, are required for robust projection of the future status of New Zealand marine ecosystems.

Ocean acidification poses a serious threat to marine calcifying organisms, yet experimental and field studies have found highly diverse responses among species and environments. Our understanding of the underlying drivers of differential responses to ocean acidification is currently limited by difficulties in directly observing and quantifying the mechanisms of bio‐calcification. Here, we present Raman spectroscopy techniques for characterizing the skeletal mineralogy and calcifying fluid chemistry of marine calcifying organisms such as corals, coralline algae, foraminifera, and fish (carbonate otoliths). First, our in vivo Raman technique is the ideal tool for investigating non‐classical mineralization pathways. This includes calcification by amorphous particle attachment, which has recently been controversially suggested as a mechanism by which corals resist the negative effects of ocean acidification. Second, high‐resolution ex vivo Raman mapping reveals complex banding structures in the mineralogy of marine calcifiers, and provides a tool to quantify calcification responses to environmental variability on various timescales from days to years. We describe the new insights into marine bio‐calcification that our techniques have already uncovered, and we consider the wide range of questions regarding calcifier responses to global change that can now be proposed and addressed with these new Raman spectroscopy tools., Newly developed in vivo and high‐resolution Raman spectroscopy analyses of marine calcifying organisms enable characterization of their mineralogy and calcification mechanisms. Insights from these new Raman spectroscopy tools are helping us understand the sensitivity of these important organisms to ocean warming and acidification.

Macroalgae are generally used as indicators of coral reef status; thus, understanding the drivers and mechanisms leading to increased macroalgal abundance are of critical importance. Ocean acidification (OA) due to elevated carbon dioxide (CO2) concentrations has been suggested to stimulate macroalgal growth and abundance on reefs. However, little is known about the physiological mechanisms by which reef macroalgae use CO2 from the bulk seawater for photosynthesis [i.e., (1) direct uptake of bicarbonate (HCO3−) and/or CO2 by means of carbon concentrating mechanisms (CCM) and (2) the diffusive uptake of CO2], which species could benefit from increased CO2 or which habitats may be more susceptible to acidification-induced algal proliferations. Here, we provide the first quantitative examination of CO2-use strategies in coral reef macroalgae and provide information on how the proportion of species and the proportional abundance of species utilising each of the carbon acquisition strategies varies across a gradient of terrestrial influence (from inshore to offshore reefs) in the Great Barrier Reef (GBR). Four macroalgal groups were identified based on their carbon uptake strategies: (1) CCM-only (HCO3− only users); (2) CCM-HCO3−/CO2 (active uptake HCO3− and/or CO2 use); (3) Non-CCM species (those relying on diffusive CO2 uptake); and (4) Calcifiers. δ13C values of macroalgae, confirmed by pH drift assays, show that diffusive CO2 use is more prevalent in deeper waters, possibly due to low light availability that limits activity of CCMs. Inshore shallow reefs had a higher proportion of CCM-only species, while reefs further away from terrestrial influence and exposed to better water quality had a higher number of non-CCM species than inshore and mid-shelf reefs. As non-CCM macroalgae are more responsive to increased seawater CO2 and OA, reef slopes of the outer reefs are probably the habitats most vulnerable to the impacts of OA. Our results suggest a potentially important role of carbon physiology in structuring macroalgal communities in the GBR.

Organisms are projected to face unprecedented rates of change in future ocean conditions due to anthropogenic climate-change. At present, marine life encounters a wide range of environmental heterogeneity from natural fluctuations to mean climate change. Manipulation studies suggest that biota from more variable marine environments have more phenotypic plasticity to tolerate environmental heterogeneity. Here, we consider current strategies employed by a range of representative organisms across various habitats - from short-lived phytoplankton to long-lived corals - in response to environmental heterogeneity. We then discuss how, if and when organismal responses (acclimate/migrate/adapt) may be altered by shifts in the magnitude of the mean climate-change signal relative to that for natural fluctuations projected for coming decades. The findings from both novel climate-change modelling simulations and prior biological manipulation studies, in which natural fluctuations are superimposed on those of mean change, provide valuable insights into organismal responses to environmental heterogeneity. Manipulations reveal that different experimental outcomes are evident between climate-change treatments which include natural fluctuations vs. those which do not. Modelling simulations project that the magnitude of climate variability, along with mean climate change, will increase in coming decades, and hence environmental heterogeneity will increase, illustrating the need for more realistic biological manipulation experiments that include natural fluctuations. However, simulations also strongly suggest that the timescales over which the mean climate-change signature will become dominant, relative to natural fluctuations, will vary for individual properties, being most rapid for CO2 (~10 years from present day) to 4 decades for nutrients. We conclude that the strategies used by biota to respond to shifts in environmental heterogeneity may be complex, as they will have to physiologically straddle wide-ranging timescales in the alteration of ocean conditions, including the need to adapt to rapidly rising CO2 and also acclimate to environmental heterogeneity in more slowly changing properties such as warming.

Natural variability in pH in the diffusive boundary layer (DBL), the discrete layer of seawater between bulk seawater and the outer surface of organisms, could be an important factor determining the response of corals and coralline algae to ocean acidification (OA). Here, two corals with different morphologies and one coralline alga were maintained under two different regimes of flow velocities, pH, and light intensities in a 12 flumes experimental system for a period of 27 weeks. We used a combination of geochemical proxies, physiological and micro-probe measurements to assess how these treatments affected the conditions in the DBL and the response of organisms to OA. Overall, low flow velocity did not ameliorate the negative effect of low pH and therefore did not provide a refugia from OA. Flow velocity had species-specific effects with positive effects on calcification for two species. pH in the calcifying fluid (pHcf) was reduced by low flow in both corals at low light only. pHcf was significantly impacted by pH in the DBL for the two species capable of significantly modifying pH in the DBL. The dissolved inorganic carbon in the calcifying fluid (DICcf) was highest under low pH for the corals and low flow for the coralline, while the saturation state in the calcifying fluid and its proxy (FWHM) were generally not affected by the treatments. This study therefore demonstrates that the effects of OA will manifest most severely in a combination of lower light and lower flow habitats for sub-tropical coralline algae. These effects will also be greatest in lower flow habitats for some corals. Together with existing literature, these findings reinforce that the effects of OA are highly context dependent, and will differ greatly between habitats, and depending on species composition.

International audience; Ocean acidification (OA) is a major threat to marine ecosystems, particularly coral reefs which are heavily reliant on calcareous species. OA decreases seawater pH and calcium carbonate saturation state (Ω), and increases the concentration of dissolved inorganic carbon (DIC). Intense scientific effort has attempted to determine the mechanisms via which ocean acidification (OA) influences calcification, led by early hypotheses that calcium carbonate saturation state (Ω) is the main driver. We grew corals and coralline algae for 8-21 weeks, under treatments where the seawater parameters Ω, pH, and DIC were manipulated to examine their differential effects on calcification rates and calcifying fluid chemistry (Ω cf , pH cf , and DIC cf). Here, using long duration experiments, we provide geochemical evidence that differing physiological controls on carbonate chemistry at the site of calcification, rather than seawater Ω, are the main determinants of calcification. We found that changes in seawater pH and DIC rather than Ω had the greatest effects on calcification and calcifying fluid chemistry, though the effects of seawater carbonate chemistry were limited. Our results demonstrate the capacity of organisms from taxa with vastly different calcification mechanisms to regulate their internal chemistry under extreme chemical conditions. These findings provide an explanation for the resistance of some species to OA, while also demonstrating how changes in seawater DIC and pH under OA influence calcification of key coral reef taxa.

Investigation of multiple stressors on a subantarctic diatom reveals the importance of considering individual and interactive effects. Experiments show that temperature and iron enrichment enhance growth and help overcome nutrient depletion.

Ocean acidification has been identified as a risk to marine ecosystems, and substantial scientific effort has been expended on investigating its effects, mostly in laboratory manipulation experiments. However, performing these manipulations correctly can be logistically difficult, and correctly designing experiments is complex, in part because of the rigorous requirements for manipulating and monitoring seawater carbonate chemistry. To assess the use of appropriate experimental design in ocean acidification research, 465 studies published between 1993 and 2014 were surveyed, focusing on the methods used to replicate experimental units. The proportion of studies that had interdependent or non-randomly interspersed treatment replicates, or did not report sufficient methodological details was 95%. Furthermore, 21% of studies did not provide any details of experimental design, 17% of studies otherwise segregated all the replicates for one treatment in one space, 15% of studies replicated CO 2 treatments in a way that made replicates more interdependent within treatments than between treatments, and 13% of studies did not report if replicates of all treatments were randomly interspersed. As a consequence, the number of experimental units used per treatment in studies was low (mean = 2.0). In a comparable analysis, there was a significant decrease in the number of published studies that employed inappropriate chemical methods of manipulating seawater (i.e. acid–base only additions) from 21 to 3%, following the release of the "Guide to best practices for ocean acidification research and data reporting" in 2010; however, no such increase in the use of appropriate replication and experimental design was observed after 2010. We provide guidelines on how to design ocean acidification laboratory experiments that incorporate the rigorous requirements for monitoring and measuring carbonate chemistry with a level of replication that increases the chances of accurate detection of biological responses to ocean acidification.

Understorey macroalgae can alter pH at their surface via metabolic activity within the concentration boundary layer (CBL), but it is unknown to what degree the presence of larger macroalgal canopies can modify the pH micro-environment of understorey species. We examined whether flow reduction by a canopy-forming macroalga could alter the thickness of the CBL at the surface of understorey crustose coralline macroalgae (CCA). This could lead to a greater metabolic influence of macroalgae on the pH and oxygen environment at the coralline’s surface. Three experimental treatments were examined in a re-circulating flume: (1) a full canopy (consisting of Carpophyllum maschalocarpum ) and understorey ( Corallina officinalis and CCA), (2) a mimic (plastic/silk) canopy plus understorey, and (3) an understorey only. Profiles of seawater velocity and pH/O 2 concentration gradients were measured at 3 bulk seawater velocities (2, 4 and 8 cm s -1 ) above the CCA in both the light and dark. Canopy macroalgae altered the pH and O 2 environment encountered by understorey coralline algae via their physical presence rather than by directly altering bulk seawater chemistry through their metabolism. Reduced seawater velocities beneath Carpophyllum and mimic canopies resulted in increased CBL thicknesses, higher pH (up to 8.9) and O 2 concentrations in the light, and lower pH (down to 7.74) and O 2 concentrations in the dark. The ability of canopies to facilitate greater metabolic changes in pH at the surface of understorey species highlights a previously unrecorded species interaction that could play an important role in influencing the physiology and ecology of understorey assemblages.

Productivity of most macroalgae is not currently considered limited by dissolved inorganic carbon (DIC), as the majority of species have CO2-concentrating mechanisms (CCM) allowing the active uptake of DIC. The alternative, diffusive uptake of CO2 (non-CCM), is considered rare (0–9 % of all macroalgal cover in a given ecosystem), and identifying species without CCMs is important in understanding factors controlling inorganic carbon use by eukaryotic algae. CCM activity has higher energetic requirements than diffusive CO2 uptake, therefore when light is low, CCM activity is reduced in favour of diffusive CO2 uptake. We hypothesized that the proportional cover of macroalgae without CCMs (red and green macroalgae) would be low (

Ocean acidification threatens the persistence of biogenic calcium carbonate (CaCO 3 ) production on coral reefs. However, some coral genera show resistance to declines in seawater pH, potentially achieved by modulating the chemistry of the fluid where calcification occurs. We use two novel geochemical techniques based on boron systematics and Raman spectroscopy, which together provide the first constraints on the sensitivity of coral calcifying fluid calcium concentrations ( ) to changing seawater pH. In response to simulated end-of-century pH conditions, Pocillopora damicornis increased to as much as 25% above that of seawater and maintained constant calcification rates. Conversely, Acropora youngei displayed less control over , and its calcification rates strongly declined at lower seawater pH. Although the role of in driving calcification has often been neglected, increasing may be a key mechanism enabling more resistant corals to cope with ocean acidification and continue to build CaCO 3 skeletons in a high-CO 2 world.

Evaluating the factors responsible for differing species-specific sensitivities to declining seawater pH is central to understanding the mechanisms via which ocean acidification (OA) affects coral calcification. We report here the results of an experiment comparing the responses of the coral Acropora yongei and Pocillopora damicornis to differing pH levels (8.09, 7.81, and 7.63) over an 8-week period. Calcification of A. youngei was reduced by 35% at pH 7.63, while calcification of P. damicornis was unaffected. The pH in the calcifying fluid (pHcf) was determined using δ11B systematics, and for both species pHcf declined slightly with seawater pH, with the decrease being more pronounced in P. damicornis. The dissolved inorganic carbon concentration at the site of calcification (DICcf) was estimated using geochemical proxies (B/Ca and δ11B) and found to be double that of seawater DIC, and increased in both species as seawater pH decreased. As a consequence, the decline of the saturation state at the site of calcification (Ωcf) with OA was partially moderated by the DICcf increase. These results highlight that while pHcf, DICcf and Ωcf are important in the mineralization process, some corals are able to maintain their calcification rates despite shifts in their calcifying fluid carbonate chemistry.

‘Multiple drivers’ (also termed ‘multiple stressors’) is the term used to describe the cumulative effects of multiple environmental factors on organisms or ecosystems. Here, we consider ocean acidification as a multiple driver because many inorganic carbon parameters are changing simultaneously, including total dissolved inorganic carbon, CO2, HCO3–, CO32–, H+ and CaCO3 saturation state. With the rapid expansion of ocean acidification research has come a greater understanding of the complexity and intricacies of how these simultaneous changes to the seawater carbonate system are affecting marine life. We start by clarifying key terms used by chemists and biologists to describe the changing seawater inorganic carbon system. Then, using key groups of non-calcifying (fish, seaweeds, diatoms) and calcifying (coralline algae, coccolithophores, corals, molluscs) organisms, we consider how various physiological processes are affected by different components of the carbonate system.

In situ effects of ocean acidification are increasingly studied at submarine CO2 vents. Here we present a preliminary investigation into the water chemistry and biology of cool temperate CO2 vents near Whakaari–White Island, New Zealand. Water samples were collected inside three vent shafts, within vents at a distance of 2m from the shaft and at control sites. Vent samples contained both seawater pH on the total scale (pHT) and carbonate saturation states that were severely reduced, creating conditions as predicted for beyond the year 2100. Vent samples showed lower salinities, higher temperatures and greater nutrient concentrations. Sulfide levels were elevated and mercury levels were at concentrations considered toxic at all vent and control sites, but stable organic and inorganic ligands were present, as deduced from Cu speciation data, potentially mediating harmful effects on local organisms. The biological investigations focused on phytoplankton, zooplankton and macroalgae. Interestingly, we found lower abundances but higher diversity of phytoplankton and zooplankton at sites in the direct vicinity of Whakaari. Follow-up studies will need a combination of methods and approaches to attribute observations to specific drivers. The Whakaari vents represent a unique ecosystem with considerable biogeochemical complexity, which, like many other vent systems globally, require care in their use as a model of ‘future oceans’.

Understanding ecosystem responses to global and local anthropogenic impacts is paramount to predicting future ecosystem states. We used an ecosystem modeling approach to investigate the independent and cumulative effects of fishing, marine protection, and ocean acidification on a coastal ecosystem. To quantify the effects of ocean acidification at the ecosystem level, we used information from the peer-reviewed literature on the effects of ocean acidification. Using an Ecopath with Ecosim ecosystem model for the Wellington south coast, including the Taputeranga Marine Reserve (MR), New Zealand, we predicted ecosystem responses under 4 scenarios: ocean acidification + fishing; ocean acidification + MR (no fishing); no ocean acidification + fishing; no ocean acidification + MR for the year 2050. Fishing had a larger effect on trophic group biomasses and trophic structure than ocean acidification, whereas the effects of ocean acidification were only large in the absence of fishing. Mortality by fishing had large, negative effects on trophic group biomasses. These effects were similar regardless of the presence of ocean acidification. Ocean acidification was predicted to indirectly benefit certain species in the MR scenario. This was because lobster (Jasus edwardsii) only recovered to 58% of the MR biomass in the ocean acidification + MR scenario, a situation that benefited the trophic groups lobsters prey on. Most trophic groups responded antagonistically to the interactive effects of ocean acidification and marine protection (46%; reduced response); however, many groups responded synergistically (33%; amplified response). Conservation and fisheries management strategies need to account for the reduced recovery potential of some exploited species under ocean acidification, nonadditive interactions of multiple factors, and indirect responses of species to ocean acidification caused by declines in calcareous predators.

The sustained absorption of anthropogenically released atmospheric CO2 by the oceans is modifying seawater carbonate chemistry, a process termed ocean acidification (OA). By the year 2100, the worst case scenario is a decline in the average oceanic surface seawater pH by 0.3 units to 7.75. The changing seawater carbonate chemistry is predicted to negatively affect many marine species, particularly calcifying organisms such as coralline algae, while species such as diatoms and fleshy seaweed are predicted to be little affected or may even benefit from OA. It has been hypothesized in previous work that the direct negative effects imposed on coralline algae, and the direct positive effects on fleshy seaweeds and diatoms under a future high CO2 ocean could result in a reduced ability of corallines to compete with diatoms and fleshy seaweed for space in the future. In a 6-week laboratory experiment, we examined the effect of pH 7.60 (pH predicted to occur due to ocean acidification just beyond the year 2100) compared to pH 8.05 (present day) on the lateral growth rates of an early successional, cold-temperate species assemblage dominated by crustose coralline algae and benthic diatoms. Crustose coralline algae and benthic diatoms maintained positive growth rates in both pH treatments. The growth rates of coralline algae were three times lower at pH 7.60, and a non-significant decline in diatom growth meant that proportions of the two functional groups remained similar over the course of the experiment. Our results do not support our hypothesis that benthic diatoms will outcompete crustose coralline algae under future pH conditions. However, while crustose coralline algae were able to maintain their presence in this benthic rocky reef species assemblage, the reduced growth rates suggest that they will be less capable of recolonizing after disturbance events, which could result in reduced coralline cover under OA conditions.

Purpose of Review We investigate whether regimes of greater daily variability in temperature or pH result in greater tolerance to ocean warming and acidification in key reef-building taxa (corals, coralline algae). Recent Findings Temperature and pH histories will likely influence responses to future warming and acidification. Past exposure of corals to increased temperature variability generally leads to greater thermotolerance. However, the effects of past pH variability are unclear. Variability in pH or temperature will likely modify responses during exposure to stressors, independent of environmental history. In the laboratory, pH variability often limited the effects of ocean acidification, but the effects of temperature variability on responses to warming were equivocal. Summary Environmental variability could alter responses of coral reef organisms to climate change. Determining how both environmental history as well as the direct impacts of environmental variability will interact with the effects of anthropogenic climate change should now be high priority.

Coralline algae provide important ecosystem services but are susceptible to the impacts of ocean acidification. However, the mechanisms are uncertain, and the magnitude is species specific. Here, we assess whether species-specific responses to ocean acidification of coralline algae are related to differences in pH at the site of calcification within the calcifying fluid/medium (pHcf ) using δ11 B as a proxy. Declines in δ11 B for all three species are consistent with shifts in δ11 B expected if B(OH)4- was incorporated during precipitation. In particular, the δ11 B ratio in Amphiroa anceps was too low to allow for reasonable pHcf values if B(OH)3 rather than B(OH)4- was directly incorporated from the calcifying fluid. This points towards δ11 B being a reliable proxy for pHcf for coralline algal calcite and that if B(OH)3 is present in detectable proportions, it can be attributed to secondary postincorporation transformation of B(OH)4- . We thus show that pHcf is elevated during calcification and that the extent is species specific. The net calcification of two species of coralline algae (Sporolithon durum, and Amphiroa anceps) declined under elevated CO2 , as did their pHcf . Neogoniolithon sp. had the highest pHcf , and most constant calcification rates, with the decrease in pHcf being ¼ that of seawater pH in the treatments, demonstrating a control of coralline algae on carbonate chemistry at their site of calcification. The discovery that coralline algae upregulate pHcf under ocean acidification is physiologically important and should be included in future models involving calcification.