85495036
pH Variability Exacerbates Effects of Ocean Acidification on a Caribbean Crustose Coralline Alga
Crustose coralline algae (CCA) are among the most sensitive marine taxa to the pH changes predicted with ocean acidification (OA). However, many CCA exist in habitats where diel cycles in pH can surpass near-future OA projections. The prevailing theory that natural variability increases the tolerance of calcifiers to OA has not been widely tested with tropical CCA. Here, we assess the response of the reef-building species Lithophyllum congestum to stable and variable pH treatments, including an ambient control (amb/stable). The amb/variable treatment simulated an ambient diel cycle in pH (7.65-7.95), OA/stable simulated constant low pH reflecting worst-case year 2100 predictions (7.7), and OA/variable combined diel cycling with lower mean pH (7.45-7.75). We monitored the effects of pH on total calcification rate and photophysiology (maximum quantum yield) over 16 weeks. To assess the potential for acclimatization, we also quantified calcification rates during the first (0-8 weeks) and second (8-16 weeks) halves of the experiment. Calcification rates were lower in all pH treatments relative to ambient controls and photophysiology was unaffected. At the end of the 16-week experiment, total calcification rates were similarly low in the amb/variable and OA/stable treatment (27-29%), whereas rates declined by double in the OA/variable treatment (60%). When comparing the first and second halves of the experiment, there was no acclimatization in stable treatments as calcification rates remained unchanged in both the amb/stable and OA/stable treatments. In contrast, calcification rates deteriorated between periods in the variable treatments: from a 16-47% reduction in the amb/variable treatment to a 49-79% reduction in the OA/variable treatment, relative to controls. Our findings provide compelling evidence that pH variability can heighten CCA sensitivity to reductions in pH. Moreover, the decline in calcification rate over time directly contrasts prevailing theory that variability inherently increases organismal tolerances to low pH, and suggests that mechanisms of tolerance may become limited with increasing time of exposure. The significant role of diel pH cycling in CCA responses to OA indicates that organisms in habitats with diel variability could respond more severely to rapid changes in ocean pH associated with OA than predicted by experiments conducted under static conditions.
12607336
Coral Reefs Under Rapid Climate Change and Ocean Acidification
Atmospheric carbon dioxide concentration is expected to exceed 500 parts per million and global temperatures to rise by at least 2°C by 2050 to 2100, values that significantly exceed those of at least the past 420,000 years during which most extant marine organisms evolved. Under conditions expected in the 21st century, global warming and ocean acidification will compromise carbonate accretion, with corals becoming increasingly rare on reef systems. The result will be less diverse reef communities and carbonate reef structures that fail to be maintained. Climate change also exacerbates local stresses from declining water quality and overexploitation of key species, driving reefs increasingly toward the tipping point for functional collapse. This review presents future scenarios for coral reefs that predict increasingly serious consequences for reef-associated fisheries, tourism, coastal protection, and people. As the International Year of the Reef 2008 begins, scaled-up management intervention and decisive action on global emissions are required if the loss of coral-dominated ecosystems is to be avoided.
4852561
Baseline Assessment of Net Calcium Carbonate Accretion Rates on U.S. Pacific Reefs
This paper presents a comprehensive quantitative baseline assessment of in situ net calcium carbonate accretion rates (g CaCO3 cm-2 yr-1) of early successional recruitment communities on Calcification Accretion Unit (CAU) plates deployed on coral reefs at 78 discrete sites, across 11 islands in the central and south Pacific Oceans. Accretion rates varied substantially within and between islands, reef zones, levels of wave exposure, and island geomorphology. For forereef sites, mean accretion rates were the highest at Rose Atoll, Jarvis, and Swains Islands, and the lowest at Johnston Atoll and Tutuila. A comparison between reef zones showed higher accretion rates on forereefs compared to lagoon sites; mean accretion rates were also higher on windward than leeward sites but only for a subset of islands. High levels of spatial variability in net carbonate accretion rates reported herein draw attention to the heterogeneity of the community assemblages. Percent cover of key early successional taxa on CAU plates did not reflect that of the mature communities present on surrounding benthos, possibly due to the short deployment period (2 years) of the experimental units. Yet, net CaCO3 accretion rates were positively correlated with crustose coralline algae (CCA) percent cover on the surrounding benthos and on the CAU plates, which on average represented >70% of the accreted material. For foreeefs and lagoon sites combined CaCO3 accretion rates were statistically correlated with total alkalinity and Chlorophyll-a; a GAM analysis indicated that SiOH and Halimeda were the best predictor variables of accretion rates on lagoon sites, and total alkalinity and Chlorophyll-a for forereef sites, demonstrating the utility of CAUs as a tool to monitor changes in reef accretion rates as they relate to ocean acidification. This study underscores the pivotal role CCA play as a key benthic component and supporting actively calcifying reefs; high Mg-calcite exoskeletons makes CCA extremely susceptible changes in ocean water pH, emphasizing the far-reaching threat that ocean acidification poses to the ecological function and persistence of coral reefs worldwide.
51950800
Integrating the Effects of Ocean Acidification across Functional Scales on Tropical Coral Reefs
There are concerns about the future of coral reefs in the face of ocean acidification and warming, and although studies of these phenomena have advanced quickly, efforts have focused on pieces of the puzzle rather than integrating them to evaluate ecosystem-level effects. The field is now poised to begin this task, but there are information gaps that first must be overcome before progress can be made. Many of these gaps focus on calcification at the levels of cells, organisms, populations, communities, and ecosystem, and their closure will be made difficult by the complexity of the interdependent processes by which coral reefs respond to ocean acidification, with effects scaling from cells to ecosystems and from microns to kilometers. Existing ecological theories provide an important and largely untapped resource for overcoming these difficulties, and they offer great potential for integrating the effects of ocean acidification across scales on coral reefs.
8090344
Re-evaluating the health of coral reef communities: baselines and evidence for human impacts across the central Pacific
Numerous studies have documented declines in the abundance of reef-building corals over the last several decades and in some but not all cases, phase shifts to dominance by macroalgae have occurred. These assessments, however, often ignore the remainder of the benthos and thus provide limited information on the present-day structure and function of coral reef communities. Here, using an unprecedentedly large dataset collected within the last 10 years across 56 islands spanning five archipelagos in the central Pacific, we examine how benthic reef communities differ in the presence and absence of human populations. Using islands as replicates, we examine whether benthic community structure is associated with human habitation within and among archipelagos and across latitude. While there was no evidence for coral to macroalgal phase shifts across our dataset we did find that the majority of reefs on inhabited islands were dominated by fleshy non-reef-building organisms (turf algae, fleshy macroalgae and non-calcifying invertebrates). By contrast, benthic communities from uninhabited islands were more variable but in general supported more calcifiers and active reef builders (stony corals and crustose coralline algae). Our results suggest that cumulative human impacts across the central Pacific may be causing a reduction in the abundance of reef builders resulting in island scale phase shifts to dominance by fleshy organisms.
20698644
Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms.
Ocean acidification is a pervasive stressor that could affect many marine organisms and cause profound ecological shifts. A variety of biological responses to ocean acidification have been measured across a range of taxa, but this information exists as case studies and has not been synthesized into meaningful comparisons amongst response variables and functional groups. We used meta-analytic techniques to explore the biological responses to ocean acidification, and found negative effects on survival, calcification, growth and reproduction. However, there was significant variation in the sensitivity of marine organisms. Calcifying organisms generally exhibited larger negative responses than non-calcifying organisms across numerous response variables, with the exception of crustaceans, which calcify but were not negatively affected. Calcification responses varied significantly amongst organisms using different mineral forms of calcium carbonate. Organisms using one of the more soluble forms of calcium carbonate (high-magnesium calcite) can be more resilient to ocean acidification than less soluble forms (calcite and aragonite). Additionally, there was variation in the sensitivities of different developmental stages, but this variation was dependent on the taxonomic group. Our analyses suggest that the biological effects of ocean acidification are generally large and negative, but the variation in sensitivity amongst organisms has important implications for ecosystem responses.
5402051
Coralline algae (Rhodophyta) in a changing world: integrating ecological, physiological, and geochemical responses to global change
Coralline algae are globally distributed benthic primary producers that secrete calcium carbonate skeletons. In the context of ocean acidification, they have received much recent attention due to the potential vulnerability of their high‐Mg calcite skeletons and their many important ecological roles. Herein, we summarize what is known about coralline algal ecology and physiology, providing context to understand their responses to global climate change. We review the impacts of these changes, including ocean acidification, rising temperatures, and pollution, on coralline algal growth and calcification. We also assess the ongoing use of coralline algae as marine climate proxies via calibration of skeletal morphology and geochemistry to environmental conditions. Finally, we indicate critical gaps in our understanding of coralline algal calcification and physiology and highlight key areas for future research. These include analytical areas that recently have become more accessible, such as resolving phylogenetic relationships at all taxonomic ranks, elucidating the genes regulating algal photosynthesis and calcification, and calibrating skeletal geochemical metrics, as well as research directions that are broadly applicable to global change ecology, such as the importance of community‐scale and long‐term experiments in stress response.
55249867
Benthic Coral Reef Calcium Carbonate Dissolution in an Acidifying Ocean
The authors of this Review argue that changes to carbonate dissolution in an acidifying ocean, which have been relatively overlooked, are potentially more important than calcification for the future accretion and survival of coral reef ecosystems.
39233912
Framework of barrier reefs threatened by ocean acidification.
To date, studies of ocean acidification (OA) on coral reefs have focused on organisms rather than communities, and the few community effects that have been addressed have focused on shallow back reef habitats. The effects of OA on outer barrier reefs, which are the most striking of coral reef habitats and are functionally and physically different from back reefs, are unknown. Using 5-m long outdoor flumes to create treatment conditions, we constructed coral reef communities comprised of calcified algae, corals, and reef pavement that were assembled to match the community structure at 17 m depth on the outer barrier reef of Moorea, French Polynesia. Communities were maintained under ambient and 1200 μatm pCO2 for 7 weeks, and net calcification rates were measured at different flow speeds. Community net calcification was significantly affected by OA, especially at night when net calcification was depressed ~78% compared to ambient pCO2 . Flow speed (2-14 cm s(-1) ) enhanced net calcification only at night under elevated pCO2 . Reef pavement also was affected by OA, with dissolution ~86% higher under elevated pCO2 compared to ambient pCO2 . These results suggest that net accretion of outer barrier reef communities will decline under OA conditions predicted within the next 100 years, largely because of increased dissolution of reef pavement. Such extensive dissolution poses a threat to the carbonate foundation of barrier reef communities.
62831287
Is Ocean Acidification an Open-Ocean Syndrome? Understanding Anthropogenic Impacts on Seawater pH
Ocean acidification due to anthropogenic CO2 emissions is a dominant driver of long-term changes in pH in the open ocean, raising concern for the future of calcifying organisms, many of which are present in coastal habitats. However, changes in pH in coastal ecosystems result from a multitude of drivers, including impacts from watershed processes, nutrient inputs, and changes in ecosystem structure and metabolism. Interaction between ocean acidification due to anthropogenic CO2 emissions and the dynamic regional to local drivers of coastal ecosystems have resulted in complex regulation of pH in coastal waters. Changes in the watershed can, for example, lead to changes in alkalinity and CO2 fluxes that, together with metabolic processes and oceanic dynamics, yield high-magnitude decadal changes of up to 0.5 units in coastal pH. Metabolism results in strong diel to seasonal fluctuations in pH, with characteristic ranges of 0.3 pH units, with metabolically intense habitats exceeding this range on a daily basis. The intense variability and multiple, complex controls on pH implies that the concept of ocean acidification due to anthropogenic CO2 emissions cannot be transposed to coastal ecosystems directly. Furthermore, in coastal ecosystems, the detection of trends towards acidification is not trivial and the attribution of these changes to anthropogenic CO2 emissions is even more problematic. Coastal ecosystems may show acidification or basification, depending on the balance between the invasion of coastal waters by anthropogenic CO2, watershed export of alkalinity, organic matter and CO2, and changes in the balance between primary production, respiration and calcification rates in response to changes in nutrient inputs and losses of ecosystem components. Hence, we contend that ocean acidification from anthropogenic CO2 is largely an open-ocean syndrome and that a concept of anthropogenic impacts on marine pH, which is applicable across the entire ocean, from coastal to open-ocean environments, provides a superior framework to consider the multiple components of the anthropogenic perturbation of marine pH trajectories. The concept of anthropogenic impacts on seawater pH acknowledges that a regional focus is necessary to predict future trajectories in the pH of coastal waters and points at opportunities to manage these trajectories locally to conserve coastal organisms vulnerable to ocean acidification.
5706452
High-Frequency Dynamics of Ocean pH: A Multi-Ecosystem Comparison
The effect of Ocean Acidification (OA) on marine biota is quasi-predictable at best. While perturbation studies, in the form of incubations under elevated pCO2, reveal sensitivities and responses of individual species, one missing link in the OA story results from a chronic lack of pH data specific to a given species' natural habitat. Here, we present a compilation of continuous, high-resolution time series of upper ocean pH, collected using autonomous sensors, over a variety of ecosystems ranging from polar to tropical, open-ocean to coastal, kelp forest to coral reef. These observations reveal a continuum of month-long pH variability with standard deviations from 0.004 to 0.277 and ranges spanning 0.024 to 1.430 pH units. The nature of the observed variability was also highly site-dependent, with characteristic diel, semi-diurnal, and stochastic patterns of varying amplitudes. These biome-specific pH signatures disclose current levels of exposure to both high and low dissolved CO2, often demonstrating that resident organisms are already experiencing pH regimes that are not predicted until 2100. Our data provide a first step toward crystallizing the biophysical link between environmental history of pH exposure and physiological resilience of marine organisms to fluctuations in seawater CO2. Knowledge of this spatial and temporal variation in seawater chemistry allows us to improve the design of OA experiments: we can test organisms with a priori expectations of their tolerance guardrails, based on their natural range of exposure. Such hypothesis-testing will provide a deeper understanding of the effects of OA. Both intuitively simple to understand and powerfully informative, these and similar comparative time series can help guide management efforts to identify areas of marine habitat that can serve as refugia to acidification as well as areas that are particularly vulnerable to future ocean change.
29161860
Coral Reef Carbonate Chemistry Variability at Different Functional Scales
There is a growing recognition for the need to understand how seawater carbonate chemistry over coral reef environments will change in a high-CO2 world to better assess the impacts of ocean acidification on these valuable ecosystems. Coral reefs modify overlying water column chemistry through biogeochemical processes reflected in thesuch as net community organic carbon production (NCP) and calcification (NCC). However, the relative importance and influence of these processes on seawater carbonate chemistry vary across multiple functional scales (defined here as space, time, and benthic community composition), and have not been fully constrained. Here, we use Bermuda as a case study to assess 1) spatiotemporal variability in physical and chemical parameters along a depth gradient at a rim reef location, 2) the spatial variability of total alkalinity (TA) and dissolved inorganic carbon (DIC) over distinct benthic habitats to infer NCC:NCP ratios (< several km2; rim reef vs seagrass and calcium carbonate (CaCO3) sediments) on diel timescales, and 3) compare how TA-DIC relationships and NCC:NCP vary as we expand functional scales from local habitats to the entire reef platform (10’s of km2) on seasonal to interannual timescales. Our results demonstrate that TA-DIC relationships were strongly driven by local benthic metabolism and community composition over diel cycles. However, as the spatial scale expanded to the reef platform, the TA-DIC relationship reflected processes that were integrated over larger spatiotemporal scales, with effects of NCC becoming increasingly more important over NCP. This study demonstrates the importance of considering drivers across multiple functional scales to constrain carbonate chemistry variability over coral reefs.
15919979
A short-term in situ CO2 enrichment experiment on Heron Island (GBR)
Ocean acidification poses multiple challenges for coral reefs on molecular to ecological scales, yet previous experimental studies of the impact of projected CO2 concentrations have mostly been done in aquarium systems with corals removed from their natural ecosystem and placed under artificial light and seawater conditions. The Coral–Proto Free Ocean Carbon Enrichment System (CP-FOCE) uses a network of sensors to monitor conditions within each flume and maintain experimental pH as an offset from environmental pH using feedback control on the injection of low pH seawater. Carbonate chemistry conditions maintained in the −0.06 and −0.22 pH offset treatments were significantly different than environmental conditions. The results from this short-term experiment suggest that the CP-FOCE is an important new experimental system to study in situ impacts of ocean acidification on coral reef ecosystems.
32679932
Ocean acidification causes ecosystem shifts via altered competitive interactions
Ocean acidification can alter competitive dynamics between species. Although calcareous species recruited and grew at similar rates to fleshy seaweeds in ambient and low pH conditions, at later stages, in low pH, they were rapidly overgrown. These results suggest that changes in competitive balance could indirectly lead to profound ecosystem changes in an acidified ocean.
85335803
Physiological responses of three temperate coralline algae from contrasting habitats to near-future ocean acidification
Coralline algae are major calcifiers of significant ecological importance in marine habitats but are among the most sensitive calcifying organisms to ocean acidification. The elevated pCO2 effects were examined in three coralline algal species living in contrasting habitats from intertidal to subtidal zones on the north-western coast of Brittany, France: (i) Corallina elongata, a branched alga found in tidal rock pools, (ii) Lithophyllum incrustans, a crustose coralline alga from the low intertidal zone, and (iii) Lithothamnion corallioides (maerl), a free-living form inhabiting the subtidal zone. Metabolic rates were assessed on specimens grown for one month at varying pCO2: 380 (current pCO2), 550, 750 and 1000 μatm (elevated pCO2). There was no pCO2 effect on gross production in C. elongata and L. incrustans but L. incrustans respiration strongly increased with elevated pCO2. L. corallioides gross production slightly increased at 1000 μatm, while respiration remained unaffected. Calcification rates decreased with pCO2 in L. incrustans (both in the light and dark) and L. corallioides (only in the light), while C. elongata calcification was unaffected. This was consistent with the lower skeletal mMg/Ca ratio of C. elongata (0.17) relative to the two other species (0.20). L. incrustans had a higher occurrence of bleaching that increased with increasing pCO2. pCO2 could indirectly impact this coralline species physiology making them more sensitive to other stresses such as diseases or pathogens. These results underlined that the physiological response of coralline algae to near-future ocean acidification is species-specific and that species experiencing naturally strong pH variations were not necessarily more resistant to elevated pCO2 than species from more stable environment.
135119924
Free Ocean CO2 Enrichment (FOCE) experiments: Scientific and technical recommendations for future in situ ocean acidification projects
Abstract Free Ocean CO2 Enrichment (FOCE) experiments are a relatively recent development in ocean acidification research, designed to address the need for in situ, long-term, community level experiments. FOCE studies have been conducted across different marine benthic habitats and regions, from Antarctica to the tropics. Based on this previous research we have formed some core operating principles that will aid those embarking on future FOCE experiments. FOCE studies have potential to provide important insight into the effects of ocean acidification that can add to or refine conclusions drawn from laboratory or single species studies because they are conducted in situ on intact assemblages. Scaling up from sub-organismal and individual effects to also include indirect impacts on the ecosystem and ecosystem services, make FOCE experiments essential in filling in current knowledge gaps in our understanding of ocean acidification. While FOCE systems are complex, relatively costly, and somewhat difficult to operate, the challenges they pose are tractable and they have proven to be a useful approach in ocean acidification research. The aim of this paper is to draw from the experiences of past FOCE experiments and provide practical advice for designing, building and operating a FOCE experiment. Some of the most important recommendations include: field testing the system design; having a backup power supply; using replicate treatment enclosures; monitoring and maintaining the chemistry appropriately; allowing sufficient time to achieve near CO2 equilibrium conditions; and having a scientific focus with a core set of hypotheses. Future FOCE experiments could focus on longer durations, multiple factors, and testing more intact benthic marine communities and ecosystems. We hope this paper will encourage further FOCE deployments and experiments, as well as provide some guidelines to improve future FOCE studies and advance ocean acidification research.
7846357
pH homeostasis during coral calcification in a free ocean CO2 enrichment (FOCE) experiment, Heron Island reef flat, Great Barrier Reef
Significance In situ free ocean CO2 enrichment (FOCE) experiments and geochemical analyses (δ11B, Sr/Ca) conducted on corals (Porites cylindrica) from the highly dynamic Heron Island reef flat of the Great Barrier Reef show that this species exerts strong physiological controls on the pH of their calcifying fluid (pHcf). Over an ∼6-mo period, from mid-winter to early summer, we show that these corals maintained their pHcf at near constant elevated levels independent of the highly variable temperatures and FOCE-controlled carbonate chemistries to which they were exposed, implying they have a high degree of tolerance to ocean acidification. Geochemical analyses (δ11B and Sr/Ca) are reported for the coral Porites cylindrica grown within a free ocean carbon enrichment (FOCE) experiment, conducted on the Heron Island reef flat (Great Barrier Reef) for a 6-mo period from June to early December 2010. The FOCE experiment was designed to simulate the effects of CO2-driven acidification predicted to occur by the end of this century (scenario RCP4.5) while simultaneously maintaining the exposure of corals to natural variations in their environment under in situ conditions. Analyses of skeletal growth (measured from extension rates and skeletal density) showed no systematic differences between low-pH FOCE treatments (ΔpH = ∼−0.05 to −0.25 units below ambient) and present day controls (ΔpH = 0) for calcification rates or the pH of the calcifying fluid (pHcf); the latter was derived from boron isotopic compositions (δ11B) of the coral skeleton. Furthermore, individual nubbins exhibited near constant δ11B compositions along their primary apical growth axes (±0.02 pHcf units) regardless of the season or treatment. Thus, under the highly dynamic conditions of the Heron Island reef flat, P. cylindrica up-regulated the pH of its calcifying fluid (pHcf ∼8.4–8.6), with each nubbin having near-constant pHcf values independent of the large natural seasonal fluctuations of the reef flat waters (pH ∼7.7 to ∼8.3) or the superimposed FOCE treatments. This newly discovered phenomenon of pH homeostasis during calcification indicates that coral living in highly dynamic environments exert strong physiological controls on the carbonate chemistry of their calcifying fluid, implying a high degree of resilience to ocean acidification within the investigated ranges.
134299736
The Role of Natural Variability in Shaping the Response of Coral Reef Organisms to Climate Change
Purpose of ReviewWe 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 FindingsTemperature 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.SummaryEnvironmental 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.
4974496
Species-specific responses to ocean acidification should account for local adaptation and adaptive plasticity
Global stressors, such as ocean acidification, constitute a rapidly emerging and significant problem for marine organisms, ecosystem functioning and services. The coastal ecosystems of the Humboldt Current System (HCS) off Chile harbour a broad physical–chemical latitudinal and temporal gradient with considerable patchiness in local oceanographic conditions. This heterogeneity may, in turn, modulate the specific tolerances of organisms to climate stress in species with populations distributed along this environmental gradient. Negative response ratios are observed in species models (mussels, gastropods and planktonic copepods) exposed to changes in the partial pressure of CO2 (pCO2) far from the average and extreme pCO2 levels experienced in their native habitats. This variability in response between populations reveals the potential role of local adaptation and/or adaptive phenotypic plasticity in increasing resilience of species to environmental change. The growing use of standard ocean acidification scenarios and treatment levels in experimental protocols brings with it a danger that inter-population differences are confounded by the varying environmental conditions naturally experienced by different populations. Here, we propose the use of a simple index taking into account the natural pCO2 variability, for a better interpretation of the potential consequences of ocean acidification on species inhabiting variable coastal ecosystems. Using scenarios that take into account the natural variability will allow understanding of the limits to plasticity across organismal traits, populations and species.
24288198
Biological responses to environmental heterogeneity under future ocean conditions.
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.
2015086
Building coral reef resilience through assisted evolution
The genetic enhancement of wild animals and plants for characteristics that benefit human populations has been practiced for thousands of years, resulting in impressive improvements in commercially valuable species. Despite these benefits, genetic manipulations are rarely considered for noncommercial purposes, such as conservation and restoration initiatives. Over the last century, humans have driven global climate change through industrialization and the release of increasing amounts of CO2, resulting in shifts in ocean temperature, ocean chemistry, and sea level, as well as increasing frequency of storms, all of which can profoundly impact marine ecosystems. Coral reefs are highly diverse ecosystems that have suffered massive declines in health and abundance as a result of these and other direct anthropogenic disturbances. There is great concern that the high rates, magnitudes, and complexity of environmental change are overwhelming the intrinsic capacity of corals to adapt and survive. Although it is important to address the root causes of changing climate, it is also prudent to explore the potential to augment the capacity of reef organisms to tolerate stress and to facilitate recovery after disturbances. Here, we review the risks and benefits of the improvement of natural and commercial stocks in noncoral reef systems and advocate a series of experiments to determine the feasibility of developing coral stocks with enhanced stress tolerance through the acceleration of naturally occurring processes, an approach known as (human)-assisted evolution, while at the same time initiating a public dialogue on the risks and benefits of this approach.
29705237
The effects of a variable temperature regime on the physiology of the reef-building coral Seriatopora hystrix: results from a laboratory-based reciprocal transplant
SUMMARY To understand the effects of global climate change on reef-building corals, a thorough investigation of their physiological mechanisms of acclimatization is warranted. However, static temperature manipulations may underestimate the thermal complexity of the reefs in which many corals live. For instance, corals of Houbihu, Taiwan, experience changes in temperature of up to 10°C over the course of a day during spring-tide upwelling events. To better understand the phenotypic plasticity of these corals, a laboratory-based experiment was conducted whereby specimens of Seriatopora hystrix from an upwelling reef (Houbihu) and conspecifics from a non-upwelling reef (Houwan) were exposed to both a stable seawater temperature (26°C) regime and a regime characterized by a 6°C fluctuation (23–29°C) over a 12 h period for 7 days. A suite of physiological and molecular parameters was measured in samples of both treatments, as well as in experimental controls, to determine site of origin (SO) and temperature treatment (TT) responses. Only chlorophyll a (chl a) concentration and growth demonstrated the hypothesized trend of higher levels when exposed to a TT that mimicked SO conditions. In contrast, chl a, maximum dark-adapted quantum yield of photosystem II (Fv/Fm), and Symbiodinium ribulose-1,5-bisphosphate carboxylase/oxygenase (rbcL), photosystem I (psI, subunit III) and phosphoglycolate phosphatase (pgpase) mRNA expression demonstrated significant TT effects. Specifically, levels of these response variables were higher in samples exposed to a variable temperature regime, suggesting that S. hystrix may acclimate to fluctuating temperatures by increasing its capacity for photosynthesis.
4573099
Acclimatization of the Crustose Coralline Alga Porolithon onkodes to Variable pCO2
Ocean acidification (OA) has important implications for the persistence of coral reef ecosystems, due to potentially negative effects on biomineralization. Many coral reefs are dynamic with respect to carbonate chemistry, and experience fluctuations in pCO2 that exceed OA projections for the near future. To understand the influence of dynamic pCO2 on an important reef calcifier, we tested the response of the crustose coralline alga Porolithon onkodes to oscillating pCO2. Individuals were exposed to ambient (400 µatm), high (660 µatm), or variable pCO2 (oscillating between 400/660 µatm) treatments for 14 days. To explore the potential for coralline acclimatization, we collected individuals from low and high pCO2 variability sites (upstream and downstream respectively) on a back reef characterized by unidirectional water flow in Moorea, French Polynesia. We quantified the effects of treatment on algal calcification by measuring the change in buoyant weight, and on algal metabolism by conducting sealed incubations to measure rates of photosynthesis and respiration. Net photosynthesis was higher in the ambient treatment than the variable treatment, regardless of habitat origin, and there was no effect on respiration or gross photosynthesis. Exposure to high pCO2 decreased P. onkodes calcification by >70%, regardless of the original habitat. In the variable treatment, corallines from the high variability habitat calcified 42% more than corallines from the low variability habitat. The significance of the original habitat for the coralline calcification response to variable, high pCO2 indicates that individuals existing in dynamic pCO2 habitats may be acclimatized to OA within the scope of in situ variability. These results highlight the importance of accounting for natural pCO2 variability in OA manipulations, and provide insight into the potential for plasticity in habitat and species-specific responses to changing ocean chemistry.
51942498
Resistance of corals and coralline algae to ocean acidification: physiological control of calcification under natural pH variability
Ocean acidification is a threat to the continued accretion of coral reefs, though some undergo daily fluctuations in pH exceeding declines predicted by 2100. We test whether exposure to greater pH variability enhances resistance to ocean acidification for the coral Goniopora sp. and coralline alga Hydrolithon reinboldii from two sites: one with low pH variability (less than 0.15 units daily; Shell Island) and a site with high pH variability (up to 1.4 pH units daily; Tallon Island). We grew populations of both species for more than 100 days under a combination of differing pH variability (high/low) and means (ambient pH 8.05/ocean acidification pH 7.65). Calcification rates of Goniopora sp. were unaffected by the examined variables. Calcification rates of H. reinboldii were significantly faster in Tallon than in Shell Island individuals, and Tallon Island individuals calcified faster in the high variability pH 8.05 treatment compared with all others. Geochemical proxies for carbonate chemistry within the calcifying fluid (cf) of both species indicated that only mean seawater pH influenced pHcf. pH treatments had no effect on proxies for Ωcf. These limited responses to extreme pH treatments demonstrate that some calcifying taxa may be capable of maintaining constant rates of calcification under ocean acidification by actively modifying Ωcf.
4489085
Mechanisms of reef coral resistance to future climate change
Reef corals are highly sensitive to heat, yet populations resistant to climate change have recently been identified. To determine the mechanisms of temperature tolerance, we reciprocally transplanted corals between reef sites experiencing distinct temperature regimes and tested subsequent physiological and gene expression profiles. Local acclimatization and fixed effects, such as adaptation, contributed about equally to heat tolerance and are reflected in patterns of gene expression. In less than 2 years, acclimatization achieves the same heat tolerance that we would expect from strong natural selection over many generations for these long-lived organisms. Our results show both short-term acclimatory and longer-term adaptive acquisition of climate resistance. Adding these adaptive abilities to ecosystem models is likely to slow predictions of demise for coral reef ecosystems. The coral Acropora hyacinthus is capable of rapid acclimation to high temperatures [Also see Perspective by Eakin] Hot and bothered corals can cope How well can corals adapt to temperature extremes? Better than anticipated, it turns out. Corals from reef pools with wide temperature fluctuations resist stress better than corals from less extreme pools. Nevertheless, corals transplanted into the hotter and more variable conditions soon acquired thermal tolerance. Palumbi et al. (see the Perspective by Eakin) found that the tougher specimens produced more of certain proteins, such as the tumor necrosis factor receptor superfamily, which protected them from the effects of heat. Ramping up heat shock and transport proteins yielded heat tolerance far more rapidly than mutation and adaptation. Hopefully, this ability will allow some mitigation of climate change on coral reefs. Science, this issue p. 895; see also p. 798.
10596037
Coralline algal structure is more sensitive to rate, rather than the magnitude, of ocean acidification
Marine pCO2 enrichment via ocean acidification (OA), upwelling and release from carbon capture and storage (CCS) facilities is projected to have devastating impacts on marine biomineralisers and the services they provide. However, empirical studies using stable endpoint pCO2 concentrations find species exhibit variable biological and geochemical responses rather than the expected negative patterns. In addition, the carbonate chemistry of many marine systems is now being observed to be more variable than previously thought. To underpin more robust projections of future OA impacts on marine biomineralisers and their role in ecosystem service provision, we investigate coralline algal responses to realistically variable scenarios of marine pCO2 enrichment. Coralline algae are important in ecosystem function; providing habitats and nursery areas, hosting high biodiversity, stabilizing reef structures and contributing to the carbon cycle. Red coralline marine algae were exposed for 80 days to one of three pH treatments: (i) current pH (control); (ii) low pH (7.7) representing OA change; and (iii) an abrupt drop to low pH (7.7) representing the higher rates of pH change observed at natural vent systems, in areas of upwelling and during CCS releases. We demonstrate that red coralline algae respond differently to the rate and the magnitude of pH change induced by pCO2 enrichment. At low pH, coralline algae survived by increasing their calcification rates. However, when the change to low pH occurred at a fast rate we detected, using Raman spectroscopy, weaknesses in the calcite skeleton, with evidence of dissolution and molecular positional disorder. This suggests that, while coralline algae will continue to calcify, they may be structurally weakened, putting at risk the ecosystem services they provide. Notwithstanding evolutionary adaptation, the ability of coralline algae to cope with OA may thus be determined primarily by the rate, rather than magnitude, at which pCO2 enrichment occurs.
11766482
Contrasting effects of ocean acidification on tropical fleshy and calcareous algae
Despite the heightened awareness of ocean acidification (OA) effects on marine organisms, few studies empirically juxtapose biological responses to CO2 manipulations across functionally distinct primary producers, particularly benthic algae. Algal responses to OA may vary because increasing CO2 has the potential to fertilize photosynthesis but impair biomineralization. Using a series of repeated experiments on Palmyra Atoll, simulated OA effects were tested across a suite of ecologically important coral reef algae, including five fleshy and six calcareous species. Growth, calcification and photophysiology were measured for each species independently and metrics were combined from each experiment using a meta-analysis to examine overall trends across functional groups categorized as fleshy, upright calcareous, and crustose coralline algae (CCA). The magnitude of the effect of OA on algal growth response varied by species, but the direction was consistent within functional groups. Exposure to OA conditions generally enhanced growth in fleshy macroalgae, reduced net calcification in upright calcareous algae, and caused net dissolution in CCA. Additionally, three of the five fleshy seaweeds tested became reproductive upon exposure to OA conditions. There was no consistent effect of OA on algal photophysiology. Our study provides experimental evidence to support the hypothesis that OA will reduce the ability of calcareous algae to biomineralize. Further, we show that CO2 enrichment either will stimulate population or somatic growth in some species of fleshy macroalgae. Thus, our results suggest that projected OA conditions may favor non-calcifying algae and influence the relative dominance of fleshy macroalgae on reefs, perpetuating or exacerbating existing shifts in reef community structure.
49608620
Similar controls on calcification under ocean acidification across unrelated coral reef taxa
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 (Ωcf , pHcf , and DICcf ). 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.
9609795
Diel Variability in Seawater pH Relates to Calcification and Benthic Community Structure on Coral Reefs
Community structure and assembly are determined in part by environmental heterogeneity. While reef-building corals respond negatively to warming (i.e. bleaching events) and ocean acidification (OA), the extent of present-day natural variability in pH on shallow reefs and ecological consequences for benthic assemblages is unknown. We documented high resolution temporal patterns in temperature and pH from three reefs in the central Pacific and examined how these data relate to community development and net accretion rates of early successional benthic organisms. These reefs experienced substantial diel fluctuations in temperature (0.78°C) and pH (>0.2) similar to the magnitude of ‘warming’ and ‘acidification’ expected over the next century. Where daily pH within the benthic boundary layer failed to exceed pelagic climatological seasonal lows, net accretion was slower and fleshy, non-calcifying benthic organisms dominated space. Thus, key aspects of coral reef ecosystem structure and function are presently related to natural diurnal variability in pH.
10188246
Patterns in Temporal Variability of Temperature, Oxygen and pH along an Environmental Gradient in a Coral Reef
Spatial and temporal environmental variability are important drivers of ecological processes at all scales. As new tools allow the in situ exploration of individual responses to fluctuations, ecologically meaningful ways of characterizing environmental variability at organism scales are needed. We investigated the fine-scale spatial heterogeneity of high-frequency temporal variability in temperature, dissolved oxygen concentration, and pH experienced by benthic organisms in a shallow coastal coral reef. We used a spatio-temporal sampling design, consisting of 21 short-term time-series located along a reef flat-to-reef slope transect, coupled to a long-term station monitoring water column changes. Spectral analyses revealed sharp gradients in variance decomposed by frequency, as well as differences between physically-driven and biologically-reactive parameters. These results highlight the importance of environmental variance at organismal scales and present a new sampling scheme for exploring this variability in situ.
4683887
Ocean acidification over the next three centuries using a simple global climate carbon-cycle model: projections and sensitivities
Abstract. Continued oceanic uptake of anthropogenic CO2 is projected to significantly alter the chemistry of the upper oceans over the next three centuries, with potentially serious consequences for marine ecosystems. Relatively few models have the capability to make projections of ocean acidification, limiting our ability to assess the impacts and probabilities of ocean changes. In this study we examine the ability of Hector v1.1, a reduced-form global model, to project changes in the upper ocean carbonate system over the next three centuries, and quantify the model's sensitivity to parametric inputs. Hector is run under prescribed emission pathways from the Representative Concentration Pathways (RCPs) and compared to both observations and a suite of Coupled Model Intercomparison (CMIP5) model outputs. Current observations confirm that ocean acidification is already taking place, and CMIP5 models project significant changes occurring to 2300. Hector is consistent with the observational record within both the high- (> 55°) and low-latitude oceans (
93835979
Guide to best practices for ocean CO2 measurements
CHAP 1 - Introduction to the Guide 
CHAP 2 - Solution chemistry of carbon dioxide in sea water 
CHAP 3 - Quality assurance 
CHAP 4 - Recommended standard operating procedures (SOPs) 
SOP 1 - Water sampling for the parameters of the oceanic carbon dioxide system 
SOP 2 - Determination of total dissolved inorganic carbon in sea water 
SOP 3a - Determination of total alkalinity in sea water using a closed-cell titration 
SOP 3b - Determination of total alkalinity in sea water using an open-cell titration 
SOP 4 - Determination of p(CO2) in air that is in equilibrium with a discrete sample of sea water 
SOP 5 - Determination of p(CO2) in air that is in equilibrium with a continuous stream of sea water 
SOP 6a - Determination of the pH of sea water using a glass/reference electrode cell 
SOP 6b - Determination of the pH of sea water using the indicator dye m-cresol purple 
SOP 7 - Determination of dissolved organic carbon and total dissolved nitrogen in sea water 
SOP 7 en Espanol - Determinacion de carbono organico disuelto y nitrogeno total disuelto en agua de mar 
SOP 11 - Gravimetric calibration of the volume of a gas loop using water 
SOP 12 - Gravimetric calibration of volume delivered using water 
SOP 13 - Gravimetric calibration of volume contained using water 
SOP 14 - Procedure for preparing sodium carbonate solutions for the calibration of coulometric CT measurements 
SOP 21 - Applying air buoyancy corrections 
SOP 22 - Preparation of control charts 
SOP 23 - Statistical techniques used in quality assessment 
SOP 24 - Calculation of the fugacity of carbon dioxide in the pure gas or in air 
CHAP 5 - Physical and thermodynamic data 
 
Errata - to the hard copy of the Guide to best practices for ocean CO2 measurements
85669069
Short-term growth measurements of corals using an accurate buoyant weighing technique
An accurate method for determining the growth rates of the skeleton of isolated branch tips (nubbins) of corals over intervals of less than 24 h is described. The skeletal weight of the coral was estimated from its buoyant weight in seawater whose density had been accurately determined. The coral tissues accounted for between 1 and 5% of the total buoyant weight in Pocillopora verrucosa and Acropora humilis with differing relative tissue biomass. After correcting for tissue buoyant weight, predictions of skeletal weight were accurate to within 1%. The method was used to estimate the growth of sample nubbins of Porites porites of similar diameter, in 2 m of water at Discovery Bay, Jamaica. Since growth of these branch tips is apical, growth rate could be expressed without correction for the size. The mean 24 h skeletal growth rate ranged between 40 and 47 mg. Differences could be measured between day-time and night-time growth, the day: night ratio being 3.7. The method also showed that P. porites virtually ceases calcification during the 4 to 5 d periods that it becomes enclosed in a mucus tunic. Nubbins of P. porites attached to the reef at different locations showed clear differences in growth rate with depth, and between clear and turbid water sites. The growth rate of nubbins was compared with that of branch tips of whole corals by measuring the linear extension after staining with Alizarin Red S. After 3 1/2 mo, the mean linear extension was 4.1 mm in each case, indicating that the growth rate of nubbins is the same as that of branch tips of the whole colony. It is suggested that this buoyant weighing technique will find applications in laboratory experiments with calcification mechanisms and as a bioassay on reefs exposed to environmental stress.
19361052
Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals
Abstract. 'It should be clear that the upper temperature limit for life cannot be accurately defined' (Schmidt-Nielsen 1996). The thermal physiology of zooxanthellate reef corals is reviewed in this paper in the context of organismal and biochemical responses occurring during coral bleaching, with emphasis on methods of detection and interpretation of animal and algal symbiont stress. Coral bleaching, as presently defined in the literature, is a highly subjective term used to describe a variety of conditions pertaining to low symbiont densities in the coral–algal complex, including response to thermal stress. Three general types of high-temperature bleaching are defined: physiological bleaching, which may or may not include higher-than-normal temperature responses; algal-stress bleaching, involving dysfunction of symbiotic algae at high light and/or high temperatures; and animal-stress bleaching, where coral cells containing symbiotic algae are shed from the gastrodermal layer of cells. Since none of these methods of bleaching is mutually exclusive, a combination of intrusive and non-intrusive techniques is necessary to determine which mechanisms of symbiont loss are occurring. While quantification of symbiont densities, algal pigments, and coral tissue biomass provide unambiguous evidence of bleaching severity, measurements of physiological and biochemical degradation offer additional correlative evidence of temperature stress. Pulse-amplitude-modulated (PAM) fluorometry has emerged as an easy and relatively inexpensive non-invasive technique for monitoring symbiotic algal function both in situ and in the laboratory, when proper assumptions and interpretations are made. The roles of global warming, water quality, acclimation/adaptation processes, and relation to coral disease and reef heterogeneity are also discussed. A thorough understanding of the organismal responses occurring during bleaching will help explain changes in coral populations and in the coral reef community, and perhaps assist in predicting the future of reef corals and coral reefs during the next century of global climate change.
96995434
Use of active fluorescence to estimate phytoplankton photosynthesis in situ
We describe the theory and practice of estimating photosynthetic rates from light-stimulated changes in the quantum yield of chlorophyll fluorescence. By means of a pump-and-probe fluorescence technique, where weak probe flashes are used to measure the change in the quantum yield of fluorescence induced by the strong pump flash, it is possible to derive the absolute absorption cross sections for photosystem 2, the quantum yield for photochemistry, and the maximum rate of photosynthetic electron transport at light saturation. In conjunction with a semiempirical biophysical model of photosynthesis, these parameters can bc used to calculate the instantaneous rate of gross photosynthesis in situ under ambient irradiance. A profiling pump-and-probe fluorometer was constructed and interfaced with a CTD, and vertical profiles of variable fluorescence were obtained on four cruises in the northwest Atlantic Ocean. The derived photosynthetic rates were compared with concurrent estimates of production based on radiocarbon uptake. The correlation coefficient between the two estimates of primary production, normalized to Chl a, was 0.86; linear regression analysis yielded a slope of 1.06. There is a 3-4-fold range in the maximum change in the quantum yields of photochemistry and absorption cross-sections in natural phytoplankton communities. Uncertainties in the pump-and-probe-derived estimates of photosynthesis arc primarily due to temporal mismatches between instantaneous and time-integrated measures of production and in biological variability in the ratio of the number of PS2 reaction centers to total Chl a. Almost all measurements of phytoplankton photosynthesis in situ are based on the timedependent incorporation of radiocarbon into particulate matter or on changes in concentration of dissolved oxygen in the bulk fluid.
95011605
Photoecophysiology of Marine Macroalgae
Aquatic ecosystems are responsible for about half of the primary biomass production on earth and incorporate about 100 gigatons of atmospheric carbon per year (1). Because less than 0.5% of the water surface area is represented by freshwater systems, marine ecosystems have by far the largest share in productivity. Most carbon fixation is due to phytoplankton, but even though most macroalgae are restricted to coastal areas and the continental shelves they are responsible for a considerable proportion of the biomass productivity in the oceans (2). They play a role as primary producers being at the basis of an intricate food web and are of significant economic importance because several hundred thousand tons of seaweeds are harvested every year for food production and technological exploitation. While phytoplankton can move up and down in the water column (3), most macroalgae are sessile and thus restricted to their growth site (4). There they have to cope with the changing irradiance regime of solar radiation. In addition, being adapted to lower irradiances than those of unfiltered solar radiation, macroalgae face a serious light stress when exposed to higher irradiances (3). Consequently, macroalgae, as well as higher plants, have developed mechanisms to regulate their photosynthetic activity to operate under limited light supply and to protect themselves against excessive radiation (5,6). The mechanism of photoinhibition decreases the photosynthetic activity during periods of bright sunshine. This phenomenon is a reversible interruption of the photosynthetic electron transport chain (7) and facilitates thermal dissipation of excessive irradiation (8). Even higher stress will cause photodamage that is not as readily reversible as photoinhibition. Species of different algal groups show a distinctly different behavior upon irradiation (9-14), and especially the ability to cope with enhanced UV radiation varies widely among species (15-17). Therefore a broad survey is necessary to understand photosynthesis in aquatic ecosystems and its interaction with solar radiation. Typical green macroalgae
17461272
Coral reef calcifiers buffer their response to ocean acidification using both bicarbonate and carbonate
Central to evaluating the effects of ocean acidification (OA) on coral reefs is understanding how calcification is affected by the dissolution of CO2 in sea water, which causes declines in carbonate ion concentration [CO32−] and increases in bicarbonate ion concentration [HCO3−]. To address this topic, we manipulated [CO32−] and [HCO3−] to test the effects on calcification of the coral Porites rus and the alga Hydrolithon onkodes, measured from the start to the end of a 15-day incubation, as well as in the day and night. [CO32−] played a significant role in light and dark calcification of P. rus, whereas [HCO3−] mainly affected calcification in the light. Both [CO32−] and [HCO3−] had a significant effect on the calcification of H. onkodes, but the strongest relationship was found with [CO32−]. Our results show that the negative effect of declining [CO32−] on the calcification of corals and algae can be partly mitigated by the use of HCO3− for calcification and perhaps photosynthesis. These results add empirical support to two conceptual models that can form a template for further research to account for the calcification response of corals and crustose coralline algae to OA.
23277549
Diurnal fluctuations in seawater pH influence the response of a calcifying macroalga to ocean acidification
Coastal ecosystems that are characterized by kelp forests encounter daily pH fluctuations, driven by photosynthesis and respiration, which are larger than pH changes owing to ocean acidification (OA) projected for surface ocean waters by 2100. We investigated whether mimicry of biologically mediated diurnal shifts in pH—based for the first time on pH time-series measurements within a kelp forest—would offset or amplify the negative effects of OA on calcifiers. In a 40-day laboratory experiment, the calcifying coralline macroalga, Arthrocardia corymbosa, was exposed to two mean pH treatments (8.05 or 7.65). For each mean, two experimental pH manipulations were applied. In one treatment, pH was held constant. In the second treatment, pH was manipulated around the mean (as a step-function), 0.4 pH units higher during daylight and 0.4 units lower during darkness to approximate diurnal fluctuations in a kelp forest. In all cases, growth rates were lower at a reduced mean pH, and fluctuations in pH acted additively to further reduce growth. Photosynthesis, recruitment and elemental composition did not change with pH, but δ13C increased at lower mean pH. Including environmental heterogeneity in experimental design will assist with a more accurate assessment of the responses of calcifiers to OA.
4632969
Effect of Ocean Acidification and pH Fluctuations on the Growth and Development of Coralline Algal Recruits, and an Associated Benthic Algal Assemblage
Coralline algae are susceptible to the changes in the seawater carbonate system associated with ocean acidification (OA). However, the coastal environments in which corallines grow are subject to large daily pH fluctuations which may affect their responses to OA. Here, we followed the growth and development of the juvenile coralline alga Arthrocardia corymbosa, which had recruited into experimental conditions during a prior experiment, using a novel OA laboratory culture system to simulate the pH fluctuations observed within a kelp forest. Microscopic life history stages are considered more susceptible to environmental stress than adult stages; we compared the responses of newly recruited A. corymbosa to static and fluctuating seawater pH with those of their field-collected parents. Recruits were cultivated for 16 weeks under static pH 8.05 and 7.65, representing ambient and 4× preindustrial pCO2 concentrations, respectively, and two fluctuating pH treatments of daily x~ = 8.05 (daytime pH = 8.45, night-time pH = 7.65) and daily x~ = 7.65 (daytime pH = 8.05, night-time pH = 7.25). Positive growth rates of new recruits were recorded in all treatments, and were highest under static pH 8.05 and lowest under fluctuating pH 7.65. This pattern was similar to the adults’ response, except that adults had zero growth under fluctuating pH 7.65. The % dry weight of MgCO3 in calcite of the juveniles was reduced from 10% at pH 8.05 to 8% at pH 7.65, but there was no effect of pH fluctuation. A wide range of fleshy macroalgae and at least 6 species of benthic diatoms recruited across all experimental treatments, from cryptic spores associated with the adult A. corymbosa. There was no effect of experimental treatment on the growth of the benthic diatoms. On the community level, pH-sensitive species may survive lower pH in the presence of diatoms and fleshy macroalgae, whose high metabolic activity may raise the pH of the local microhabitat.
53647342
The responses of eight coral reef calcifiers to increasing partial pressure of CO2 do not exhibit a tipping point
The objective of this study was to investigate whether a tipping point exists in the calcification responses of coral reef calcifiers to CO2. We compared the effects of six partial pressures of CO2 (PCO2 ) from 28 Pa to 210 Pa on the net calcification of four corals (Acropora pulchra, Porites rus, Pocillopora damicornis, and Pavona cactus), and four calcified algae (Hydrolithon onkodes, Lithophyllum flavescens, Halimeda macroloba, and Halimeda minima). After 2 weeks of acclimation in a common environment, organisms were incubated in 12 aquaria for 2 weeks at the targeted PCO2 levels and net calcification was quantified. All eight species calcified at the highest PCO2 in which the calcium carbonate aragonite saturation state was , 1. Calcification decreased linearly as a function of increasing partial PCO2 in three corals and three algae. Overall, the decrease in net calcification as a function of decreasing pH was , 10% when ambient PCO2 (39 Pa) was doubled. The calcification responses of P. damicornis and H. macroloba were unaffected by increasing PCO2 . These results are inconsistent with the notion that coral reefs will be affected by rising PCO2 in a response characterized by a tipping point. Instead, our findings combined among taxa suggest a gradual decline in calcification will occur, but this general response includes specific cases of complete resistance to rising PCO2 . Together our results suggest that the overall response of coral reef communities to ocean acidification will be monotonic and inversely proportional to PCO2 , with reef-wide responses dependent on the species composition of calcifying taxa.
251587
Limits to the thermal tolerance of corals adapted to a highly fluctuating, naturally extreme temperature environment
Naturally extreme temperature environments can provide important insights into the processes underlying coral thermal tolerance. We determined the bleaching resistance of Acropora aspera and Dipsastraea sp. from both intertidal and subtidal environments of the naturally extreme Kimberley region in northwest Australia. Here tides of up to 10 m can cause aerial exposure of corals and temperatures as high as 37 °C that fluctuate daily by up to 7 °C. Control corals were maintained at ambient nearshore temperatures which varied diurnally by 4-5 °C, while treatment corals were exposed to similar diurnal variations and heat stress corresponding to ~20 degree heating days. All corals hosted Symbiodinium clade C independent of treatment or origin. Detailed physiological measurements showed that these corals were nevertheless highly sensitive to daily average temperatures exceeding their maximum monthly mean of ~31 °C by 1 °C for only a few days. Generally, Acropora was much more susceptible to bleaching than Dipsastraea and experienced up to 75% mortality, whereas all Dipsastraea survived. Furthermore, subtidal corals, which originated from a more thermally stable environment compared to intertidal corals, were more susceptible to bleaching. This demonstrates that while highly fluctuating temperatures enhance coral resilience to thermal stress, they do not provide immunity to extreme heat stress events.
55942151
Response of Mediterranean coralline algae to ocean acidification and elevated temperature
The effects of elevated partial pressure of CO2 (pCO2) and temperature, alone and in combination, on survival, calcification and dissolution were investigated in the crustose coralline alga Lithophyllum cabiochae. Algae were maintained in aquaria during 1 year at near-ambient conditions of irradiance, at ambient or elevated temperature ( 131C) and at ambient [ca. 400parts per million (ppm)] or elevated pCO2 (ca. 700ppm). Algal necroses appeared at the end of summer under elevated temperature first at 700ppm (60% of the thallus surface) and then at 400ppm (30%). The death of algae was observed only under elevated temperature and was two- to threefold higher under elevated pCO2. During the first month of the experiment, net calcification was significantly reduced under elevated pCO2. At the end of the summer period, net calcification decreased by 50% when both temperature and pCO2 were elevated while no effect was found under elevated temperature and elevated pCO2 alone. In autumn and winter, net calcification in healthy algae increased with increasing temperature, independently of the pCO2 level, while necroses and death in the algal population caused a net dissolution at elevated temperature and pCO2. The dissolution of dead algal thalli was affected by elevated pCO2, being two- to fourfold higher than under ambient pCO2. These results suggest that net dissolution is likely to exceed net calcification in L. cabiochae by the end of this century. This could have major consequences in terms of biodiversity and biogeochemistry in coralligenous communities dominated by these algae.
84401132
The photosynthetic characteristics of red coralline algae, determined using pulse amplitude modulation (PAM) fluorometry
Abstract Interest in red coralline algae is increasing due to their projected sensitivity to ocean acidification and their utility as palaeoenvironmental proxies. Thus, it is crucial to obtain a thorough understanding of their basic photosynthetic characteristics and appropriate techniques for use in both laboratory and in situ studies. This study provides fluorescence methodology and data for the ecologically important red coralline alga Lithothamnion glaciale using pulse amplitude modulation (PAM) fluorometry. Lithothamnion glaciale was sufficiently dark-acclimated for in situ work following 10 s of quasi-darkness, attaining 95–98% of the maximum photochemical efficiency (Fv/Fm). Rapid light curves conducted in situ and in the laboratory determined a low light adaptation, with a saturation intensity of 4.45–54.6 μmol photons m-2 s-1. Intra-thallus heterogeneity was observed between branch tips and bases (i.e., within the thallus) using a custom-made 2 mm fibre optic probe (the heterogeneity could not be detected using the standard 5 mm probe). Branch bases were lower light acclimated than the tips, with higher maximum effective quantum yield (Fq′/Fm′max) and lower non-photochemical quenching. Samples measured in May were higher light acclimated than in March, which suggests a degree of seasonal acclimation. Light history and photon irradiance levels were thus found to significantly affect the photosynthetic characteristics of L. glaciale.
15541465
Dynamic photoinhibition exhibited by red coralline algae in the red sea
BackgroundRed coralline algae are critical components of tropical reef systems, and their success and development is, at least in part, dependent on photosynthesis. However, natural variability in the photosynthetic characteristics of red coralline algae is poorly understood. This study investigated diurnal variability in encrusting Porolithon sp. and free-living Lithophyllum kotschyanum. Measured parameters included: photosynthetic characteristics, pigment composition, thallus reflectance and intracellular concentrations of dimethylsulphoniopropionate (DMSP), an algal antioxidant that is derived from methionine, an indirect product of photosynthesis. L. kotschyanum thalli were characterised by a bleached topside and a pigmented underside.ResultsMinimum saturation intensity and intracellular DMSP concentrations in Porolithon sp. were characterised by significant diurnal patterns in response to the high-light regime. A smaller diurnal pattern in minimum saturation intensity in the topside of L. kotschyanum was also evident. The overall reflectance of the topside of L. kotschyanum also exhibited a diurnal pattern, becoming increasingly reflective with increasing ambient irradiance. The underside of L. kotschyanum, which is shaded from ambient light exposure, exhibited a much smaller diurnal variability.ConclusionsThis study highlights a number of dynamic photoinhibition strategies adopted by coralline algae, enabling them to tolerate, rather than be inhibited by, the naturally high irradiance of tropical reef systems; a factor that may become more important in the future under global change projections. In this context, this research has significant implications for tropical reef management planning and conservation monitoring, which, if natural variability is not taken into account, may become flawed. The information provided by this research may be used to inform future investigations into the contribution of coralline algae to reef accretion, ecosystem service provision and palaeoenvironmental reconstruction.
84609751
Photosynthesis and calcification in the articulated coralline red algae Amphiroa anceps and A. foliacea
Net photosynthetic oxygen evolution in Amphiroa anceps (Lamarck) Decaisne is inhibited at high oxygen concentrations. Photosynthesis is highest between pH 6.5 and 7.5. At pH 9 to 10 there is still a significant photosynthetic rate, suggesting that this alga can use HCO-3as a substrate for photosynthesis. At pH 7.0 to 8.5, the photosynthetic rate saturates at a total inorganic carbon concentration (ΣCi) greater than 3 mM. At pH 8.5 and 8.8, calcification rate continues to increase with increasing concentration of ΣCi. Between pH 7 and 9, the calcification rate in the light in A. foliacea Lamouroux is proportional to the photosynthetic rate, whereas at higher pH where the photosynthetic rate is very low, the calcification rate is stimulated by the higher concentration of CO2-3ion. At all pH values examined, the calcification rate of living plants in the dark and of dead plants is directly proportional to the CO2-3ion concentration, suggesting little metabolic involvement in calcification processes in the dark, whereas calcification in live A. foliacea in the light is influenced both by the photosynthetic rate and the CO2-3 ion concentration in the medium.
29953481
Photosynthetic Unit Organization in a Red Alga : Relationships between Light-Harvesting Pigments and Reaction Centers.
The relative concentration of biliproteins, phycobilisomes, chlorophyll a, and reaction centers I and II are reported for Neoagardhiella bailyei, a macrophytic red alga collected in the field and compared with Anacystis nidulans, a cyanobacterium cultured in the laboratory. The ratios of chlorophyll to reaction center I, of chlorophyll to reaction center II, and the mass of phycobiliprotein per reaction center II are quite similar in Neoagardhiella and Anacystis, supporting the concept that the red algal chloroplast is derived from a cyanobacterial progenitor. The ratios of reaction center I to reaction center II are about 2.3 in both species. The Anacystis phycobilisome has about 40% of the mass of the Neoagardhiella phycobilisome, 4.9 and 14.9 x 10(6) daltons, respectively. The reaction center II/phycobilisome ratio is about 1.7 in Anacystis and 4.1 in Neoagardhiella. Phycobilisome size and physical restrictions on phycobilisome packing may be a major constraint on the reaction center II-phycobilisome association and the assembly of the photosynthetic membrane in both the red algae and cyanobacteria.
8302460
Climate change and ocean acidification effects on seagrasses and marine macroalgae.
Although seagrasses and marine macroalgae (macro-autotrophs) play critical ecological roles in reef, lagoon, coastal and open-water ecosystems, their response to ocean acidification (OA) and climate change is not well understood. In this review, we examine marine macro-autotroph biochemistry and physiology relevant to their response to elevated dissolved inorganic carbon [DIC], carbon dioxide [CO2 ], and lower carbonate [CO3 (2-) ] and pH. We also explore the effects of increasing temperature under climate change and the interactions of elevated temperature and [CO2 ]. Finally, recommendations are made for future research based on this synthesis. A literature review of >100 species revealed that marine macro-autotroph photosynthesis is overwhelmingly C3 (≥ 85%) with most species capable of utilizing HCO3 (-) ; however, most are not saturated at current ocean [DIC]. These results, and the presence of CO2 -only users, lead us to conclude that photosynthetic and growth rates of marine macro-autotrophs are likely to increase under elevated [CO2 ] similar to terrestrial C3 species. In the tropics, many species live close to their thermal limits and will have to up-regulate stress-response systems to tolerate sublethal temperature exposures with climate change, whereas elevated [CO2 ] effects on thermal acclimation are unknown. Fundamental linkages between elevated [CO2 ] and temperature on photorespiration, enzyme systems, carbohydrate production, and calcification dictate the need to consider these two parameters simultaneously. Relevant to calcifiers, elevated [CO2 ] lowers net calcification and this effect is amplified by high temperature. Although the mechanisms are not clear, OA likely disrupts diffusion and transport systems of H(+) and DIC. These fluxes control micro-environments that promote calcification over dissolution and may be more important than CaCO3 mineralogy in predicting macroalgal responses to OA. Calcareous macroalgae are highly vulnerable to OA, and it is likely that fleshy macroalgae will dominate in a higher CO2 ocean; therefore, it is critical to elucidate the research gaps identified in this review.
51623720
Nitrogen enrichment offsets direct negative effects of ocean acidification on a reef-building crustose coralline alga
Ocean acidification (OA) and nutrient enrichment threaten the persistence of near shore ecosystems, yet little is known about their combined effects on marine organisms. Here, we show that a threefold increase in nitrogen concentrations, simulating enrichment due to coastal eutrophication or consumer excretions, offset the direct negative effects of near-future OA on calcification and photophysiology of the reef-building crustose coralline alga, Porolithon onkodes. Projected near-future pCO2 levels (approx. 850 µatm) decreased calcification by 30% relative to ambient conditions. Conversely, nitrogen enrichment (nitrate + nitrite and ammonium) increased calcification by 90–130% in ambient and high pCO2 treatments, respectively. pCO2 and nitrogen enrichment interactively affected instantaneous photophysiology, with highest relative electron transport rates under high pCO2 and high nitrogen. Nitrogen enrichment alone increased concentrations of the photosynthetic pigments chlorophyll a, phycocyanin and phycoerythrin by approximately 80–450%, regardless of pCO2. These results demonstrate that nutrient enrichment can mediate direct organismal responses to OA. In natural systems, however, such direct benefits may be counteracted by simultaneous increases in negative indirect effects, such as heightened competition. Experiments exploring the effects of multiple stressors are increasingly becoming important for improving our ability to understand the ramifications of local and global change stressors in near shore ecosystems.
16202712
Ocean acidification causes bleaching and productivity loss in coral reef builders
Ocean acidification represents a key threat to coral reefs by reducing the calcification rate of framework builders. In addition, acidification is likely to affect the relationship between corals and their symbiotic dinoflagellates and the productivity of this association. However, little is known about how acidification impacts on the physiology of reef builders and how acidification interacts with warming. Here, we report on an 8-week study that compared bleaching, productivity, and calcification responses of crustose coralline algae (CCA) and branching (Acropora) and massive (Porites) coral species in response to acidification and warming. Using a 30-tank experimental system, we manipulated CO2 levels to simulate doubling and three- to fourfold increases [Intergovernmental Panel on Climate Change (IPCC) projection categories IV and VI] relative to present-day levels under cool and warm scenarios. Results indicated that high CO2 is a bleaching agent for corals and CCA under high irradiance, acting synergistically with warming to lower thermal bleaching thresholds. We propose that CO2 induces bleaching via its impact on photoprotective mechanisms of the photosystems. Overall, acidification impacted more strongly on bleaching and productivity than on calcification. Interestingly, the intermediate, warm CO2 scenario led to a 30% increase in productivity in Acropora, whereas high CO2 lead to zero productivity in both corals. CCA were most sensitive to acidification, with high CO2 leading to negative productivity and high rates of net dissolution. Our findings suggest that sensitive reef-building species such as CCA may be pushed beyond their thresholds for growth and survival within the next few decades whereas corals will show delayed and mixed responses.
10037960
TESTING THE EFFECTS OF OCEAN ACIDIFICATION ON ALGAL METABOLISM: CONSIDERATIONS FOR EXPERIMENTAL DESIGNS 1
Ocean acidification describes changes in the carbonate chemistry of the ocean due to the increased absorption of anthropogenically released CO2. Experiments to elucidate the biological effects of ocean acidification on algae are not straightforward because when pH is altered, the carbon speciation in seawater is altered, which has implications for photosynthesis and, for calcifying algae, calcification. Furthermore, photosynthesis, respiration, and calcification will themselves alter the pH of the seawater medium. In this review, algal physiologists and seawater carbonate chemists combine their knowledge to provide the fundamental information on carbon physiology and seawater carbonate chemistry required to comprehend the complexities of how ocean acidification might affect algae metabolism. A wide range in responses of algae to ocean acidification has been observed, which may be explained by differences in algal physiology, timescales of the responses measured, study duration, and the method employed to alter pH. Two methods have been widely used in a range of experimental systems: CO2 bubbling and HCl/NaOH additions. These methods affect the speciation of carbonate ions in the culture medium differently; we discuss how this could influence the biological responses of algae and suggest a third method based on HCl/NaHCO3 additions. We then discuss eight key points that should be considered prior to setting up experiments, including which method of manipulating pH to choose, monitoring during experiments, techniques for adding acidified seawater, biological side effects, and other environmental factors. Finally, we consider incubation timescales and prior conditioning of algae in terms of regulation, acclimation, and adaptation to ocean acidification.