Effects of ocean acidification on sponge communities

The effects of ocean acidification on lower invertebrates such as sponges may be pronounced because of their low capacity for acid-base regulation. However, so far, most studies have focused on calcifiers. We present the first study of the effects of ocean acidification on the Porifera. Sponge species composition and cover along pH gradients at CO2 vents off Ischia (Tyrrhenian Sea, Italy) was measured at sites with normal pH (8.1-8.2), lowered pH (mean 7.8-7.9, min 7.4-7.5) and extremely low pH (6.6). There was a strong correlation between pH and both sponge cover and species composition. Crambe crambe was the only species present in any abundance in the areas with mean pH 6.6, seven species were present at mean pH 7.8-7.9 and four species (Phorbas tenacior, Petrosia ficiformis, Chondrilla nucula and Hemimycale columella) were restricted to sites with normal pH. Sponge percentage cover decreased significantly from normal to acidified sites. No significant effect of increasing CO2 levels and decreasing pH was found on spicule form in Crambe crambe. This study indicates that increasing CO2 concentrations will likely affect sponge community composition as some demosponge species appear to be more vulnerable than others. Further research into the mechanisms by which acidification affects sponges would be useful in predicting likely effects on sessile marine communities.

Impact of elevated pCO2 on paralytic shellfish poisoning toxin content and composition in Alexandrium tamarense

Ocean acidification is considered a major threat to marine ecosystems and may particularly affect primary producers. Here we investigated the impact of elevated pCO2 on paralytic shellfish poisoning toxin (PST) content and composition in two strains of Alexandrium tamarense, Alex5 and Alex2. Experiments were carried out as dilute batch to keep carbonate chemistry unaltered over time. We observed only minor changes with respect to growth and elemental composition in response to elevated pCO2. For both strains, the cellular PST content, and in particular the associated cellular toxicity, was lower in the high CO2 treatments. In addition, Alex5 showed a shift in its PST composition from a nonsulfated analogue towards less toxic sulfated analogues with increasing pCO2. Transcriptomic analyses suggest that the ability of A. tamarense to maintain cellular homeostasis is predominantly regulated on the post-translational level rather than on the transcriptomic level. Furthermore, genes associated to secondary metabolite and amino acid metabolism in Alex5 were down-regulated in the high CO2 treatment, which may explain the lower PST content. Elevated pCO2 also induced up-regulation of a putative sulfotransferase sxtN homologue and a substantial down-regulation of several sulfatases. Such changes in sulfur metabolism may explain the shift in PST composition towards more sulfated analogues. All in all, our results indicate that elevated pCO2 will have minor consequences for growth and elemental composition, but may potentially reduce the cellular toxicity of A. tamarense.

Seawater carbonate chemistry and phytoplankton and eubacterial community compositions in the northwest subarctic Pacific

On-deck CO2-Fe-manipulated incubation experiments were conducted using surface seawater collected from the Western Subarctic Gyre of the NW Pacific in the summer of 2008 to elucidate the impacts of ocean acidification and Fe enrichment on the abundance and community composition of phytoplankton and eubacteria in the study area. During the incubation, excluding the initial period, the mean partial pressures of CO2 in non-Fe-added bottles were 230, 419, 843, and 1124 µatm, whereas those in Fe-added treatments were 152, 394, 791, and 1008 µatm. Changes in the abundance and community composition of phytoplankton were estimated using HPLC pigment signatures with the program CHEMTAX and flow cytometry. A DGGE fingerprint technique targeting 16S rRNA gene fragments was also used to estimate changes in eubacterial phylotypes during incubation. The Fe addition induced diatom blooms, and subsequently stimulated the growth of heterotrophic bacteria such as Roseobacter, Phaeobacter, and Alteromonas in the post-bloom phase. In both the Fe-limited and Fe-replete treatments, concentrations of 19'-hexanoyloxyfucoxanthin, a haptophyte marker, and the cell abundance of coccolithophores decreased at higher CO2 levels (750 and 1000 ppm), whereas diatoms exhibited little response to the changes in CO2 availability. The abundances of Synechococcus and small eukaryotic phytoplankton (<10 µm) increased at the higher CO2 levels. DGGE band positions revealed that Methylobacterium of Alphaproteobacteria occurred solely at lower CO2 levels (180 and 380 ppm) during the post-bloom phase. These results suggest that increases in CO2 level could affect not only the community composition of phytoplankton but also that of eubacteria. As these microorganisms play critical roles in the biological carbon pump and microbial loop, our results indicate that the progression of ocean acidification can alter the biogeochemical processes in the study area.

Seawater carbonate chemistry, the abiotic conditions in the fluid surrounding the embryo, growth, calcification of the cuttlefish Sepia officinalis in a laboratory experiment

This study investigated the effects of seawater pH (i.e., 8.10, 7.85 and 7.60) and temperature (16 and 19 °C) on (a) the abiotic conditions in the fluid surrounding the embryo (viz. the perivitelline fluid), (b) growth, development and (c) cuttlebone calcification of embryonic and juvenile stages of the cephalopod Sepia officinalis. Egg swelling increased in response to acidification or warming, leading to an increase in egg surface while the interactive effects suggested a limited plasticity of the swelling modulation. Embryos experienced elevated pCO2 conditions in the perivitelline fluid (>3-fold higher pCO2 than that of ambient seawater), rendering the medium under-saturated even under ambient conditions. The growth of both embryos and juveniles was unaffected by pH, whereas 45Ca incorporation in cuttlebone increased significantly with decreasing pH at both temperatures. This phenomenon of hypercalcification is limited to only a number of animals but does not guarantee functional performance and calls for better mechanistic understanding of calcification processes.

Selective mortality associated with variation in CO2 tolerance in a marine fish

Predicted future CO2 levels can affect reproduction, growth, and behaviour of many marine organisms. However, the capacity of species to adapt to predicted changes in ocean chemistry is largely unknown. We used a unique field-based experiment to test for differential survival associated with variation in CO2 tolerance in a wild population of coral-reef fishes. Juvenile damselfish exhibited variation in their response to elevated (700 µatm) CO2 when tested in the laboratory and this influenced their behaviour and risk of mortality in the wild. Individuals that were sensitive to elevated CO2 were more active and move further from shelter in natural coral reef habitat and, as a result, mortality from predation was significantly higher compared with individuals from the same treatment that were tolerant of elevated CO2. If individual variation in CO2 tolerance is heritable, this selection of phenotypes tolerant to elevated CO2 could potentially help mitigate the effects of ocean acidification.

Have we been underestimating the effects of ocean acidification in zooplankton?

Understanding how copepods may respond to ocean acidification (OA) is critical for risk assessments of ocean ecology and biogeochemistry. The perception that copepods are insensitive to OA is largely based on experiments with adult females. Their apparent resilience to increased carbon dioxide (pCO2) concentrations has supported the view that copepods are 'winners' under OA. Here, we show that this conclusion is not robust, that sensitivity across different life stages is significantly misrepresented by studies solely using adult females. Stage-specific responses to pCO2 (385-6000 µatm) were studied across different life stages of a calanoid copepod, monitoring for lethal and sublethal responses. Mortality rates varied significantly across the different life stages, with nauplii showing the highest lethal effects; nauplii mortality rates increased threefold when pCO2 concentrations reached 1000 µatm (year 2100 scenario) with LC50 at 1084 µatm pCO2. In comparison, eggs, early copepodite stages, and adult males and females were not affected lethally until pCO2 concentrations >= 3000 µatm. Adverse effects on reproduction were found, with >35% decline in nauplii recruitment at 1000 µatm pCO2. This suppression of reproductive scope, coupled with the decreased survival of early stage progeny at this pCO2 concentration, has clear potential to damage population growth dynamics in this species. The disparity in responses seen across the different developmental stages emphasizes the need for a holistic life-cycle approach to make species-level projections to climate change. Significant misrepresentation and error propagation can develop from studies which attempt to project outcomes to future OA conditions solely based on single life history stage exposures.

Seawater carbonate chemistry, survival rate, shell mass growth, shell dissolution and locomotory speed of Limacina retroversa in a laboratory experiment

Anthropogenic carbon dioxide emissions induce ocean acidification, thereby reducing carbonate ion concentration, which may affect the ability of calcifying organisms to build shells. Pteropods, the main planktonic producers of aragonite in the worlds' oceans, may be particularly vulnerable to changes in sea water chemistry. The negative effects are expected to be most severe at high-latitudes, where natural carbonate ion concentrations are low. In this study we investigated the combined effects of ocean acidification and freshening on Limacina retroversa, the dominant pteropod in sub polar areas. Living L. retroversa, collected in Northern Norwegian Sea, were exposed to four different pH values ranging from the pre-industrial level to the forecasted end of century ocean acidification scenario. Since over the past half-century the Norwegian Sea has experienced a progressive freshening with time, each pH level was combined with a salinity gradient in two factorial, randomized experiments investigating shell degradation, swimming behavior and survival. In addition, to investigate shell degradation without any physiologic influence, one perturbation experiments using only shells of dead pteropods was performed. Lower pH reduced shell mass whereas shell dissolution increased with pCO2. Interestingly, shells of dead organisms had a higher degree of dissolution than shells of living individuals. Mortality of Limacina retroversa was strongly affected only when both pH and salinity reduced simultaneously. The combined effects of lower salinity and lower pH also affected negatively the ability of pteropods to swim upwards. Results suggest that the energy cost of maintaining ion balance and avoiding sinking (in low salinity scenario) combined with the extra energy cost necessary to counteract shell dissolution (in high pCO2 scenario), exceed the available energy budget of this organism causing the pteropods to change swimming behavior and begin to collapse. Since L. retroversa play an important role in the transport of carbonates to the deep oceans these findings have significant implications for the mechanisms influencing the inorganic carbon cycle in the sub-polar area.

Seawater carbonate chemistry and carbon allocation, growth and morphology of the coccolithophore Emiliania huxleyi (calcifying strain CCMP 371) during experiments, 2011

Coccolithophores are unicellular phytoplankton that produce calcium carbonate coccoliths as an exoskeleton. Emiliania huxleyi, the most abundant coccolithophore in the world's ocean, plays a major role in the global carbon cycle by regulating the exchange of CO2 across the ocean-atmosphere interface through photosynthesis and calcium carbonate precipitation. As CO2 concentration is rising in the atmosphere, the ocean is acidifying and ammonium (NH4) concentration of future ocean water is expected to rise. The latter is attributed to increasing anthropogenic nitrogen (N) deposition, increasing rates of cyanobacterial N2 fixation due to warmer and more stratified oceans, and decreased rates of nitrification due to ocean acidification. Thus future global climate change will cause oceanic phytoplankton to experience changes in multiple environmental parameters including CO2, pH, temperature and nitrogen source. This study reports on the combined effect of elevated pCO2 and increased NH4 to nitrate (NO3) ratio (NH4/NO3) on E. huxleyi, maintained in continuous cultures for more than 200 generations under two pCO2 levels and two different N sources. Here we show that NH4 assimilation under N-replete conditions depresses calcification at both low and high pCO2, alters coccolith morphology, and increases primary production. We observed that N source and pCO2 synergistically drive growth rates, cell size and the ratio of inorganic to organic carbon. These responses to N source suggest that, compared to increasing CO2 alone, a greater disruption of the organic carbon pump could be expected in response to the combined effect of increased NH4/NO3 ratio and CO2 level in the future acidified ocean. Additional experiments conducted under lower nutrient conditions are needed prior to extrapolating our findings to the global oceans. Nonetheless, our results emphasize the need to assess combined effects of multiple environmental parameters on phytoplankton biology in order to develop accurate predictions of phytoplankton responses to ocean acidification.

Ocean acidification induces multi-generational decline in copepod naupliar production with possible conflict for reproductive resource allocation

Climate change, including ocean acidification (OA), presents fundamental challenges to marine biodiversity and sustained ecosystem health. We determined reproductive response (measured as naupliar production), cuticle composition and stage specific growth of the copepod Tisbe battagliai over three generations at four pH conditions (pH 7.67, 7.82, 7.95, and 8.06). Naupliar production increased significantly at pH 7.95 compared with pH 8.06 followed by a decline at pH 7.82. Naupliar production at pH 7.67 was higher than pH 7.82. We attribute the increase at pH 7.95 to an initial stress response which was succeeded by a hormesis-like response at pH 7.67. A multi-generational modelling approach predicted a gradual decline in naupliar production over the next 100 years (equivalent to approximately 2430 generations). There was a significant growth reduction (mean length integrated across developmental stage) relative to controls. There was a significant increase in the proportion of carbon relative to oxygen within the cuticle as seawater pH decreased. Changes in growth, cuticle composition and naupliar production strongly suggest that copepods subjected to OA-induced stress preferentially reallocate resources towards maintaining reproductive output at the expense of somatic growth and cuticle composition. These responses may drive shifts in life history strategies that favour smaller brood sizes, females and perhaps later maturing females, with the potential to profoundly destabilise marine trophodynamics.

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.

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.

Trace element profiles of the sea anemone Anemonia viridis living nearby a natural CO2 vent

Ocean acidification (OA) is not an isolated threat, but acts in concert with other impacts on ecosystems and species. Coastal marine invertebrates will have to face the synergistic interactions of OA with other global and local stressors. One local factor, common in coastal environments, is trace element contamination. CO2 vent sites are extensively studied in the context of OA and are often considered analogous to the oceans in the next few decades. The CO2 vent found at Levante Bay (Vulcano, NE Sicily, Italy) also releases high concentrations of trace elements to its surrounding seawater, and is therefore a unique site to examine the effects of long-term exposure of nearby organisms to high pCO2 and trace element enrichment in situ. The sea anemone Anemonia viridis is prevalent next to the Vulcano vent and does not show signs of trace element poisoning/stress. The aim of our study was to compare A. viridis trace element profiles and compartmentalization between high pCO2 and control environments. Rather than examining whole anemone tissue, we analyzed two different body compartments-the pedal disc and the tentacles, and also examined the distribution of trace elements in the tentacles between the animal and the symbiotic algae. We found dramatic changes in trace element tissue concentrations between the high pCO2/high trace element and control sites, with strong accumulation of iron, lead, copper and cobalt, but decreased concentrations of cadmium, zinc and arsenic proximate to the vent. The pedal disc contained substantially more trace elements than the anemone's tentacles, suggesting the pedal disc may serve as a detoxification/storage site for excess trace elements. Within the tentacles, the various trace elements displayed different partitioning patterns between animal tissue and algal symbionts. At both sites iron was found primarily in the algae, whereas cadmium, zinc and arsenic were primarily found in the animal tissue. Our data suggests that A. viridis regulates its internal trace element concentrations by compartmentalization and excretion and that these features contribute to its resilience and potential success at the trace element-rich high pCO2 vent.

Sensitivity to ocean acidification parallels natural pCO2 gradients experienced by Arctic copepods under winter sea ice

The Arctic Ocean is a bellwether for ocean acidification, yet few direct Arctic studies have been carried out and limited observations exist, especially in winter. We present unique under-ice physicochemical data showing the persistence of a mid water column area of high CO2 and low pH through late winter, Zooplankton data demonstrating that the dominant copepod species are distributed across these different physicochemical conditions, and empirical data demonstrating that these copepods show sensitivity to pCO2 that parallels the range of natural pCO2 they experience through their daily vertical migration behavior. Our data, collected as part of the Catlin Arctic Survey, provide unique insight into the link between environmental variability, behavior, and an organism's physiological tolerance to CO2 in key Arctic biota.

Hysteresis between coral reef calcification and the seawater aragonite saturation state

Some predictions of how ocean acidification (OA) will affect coral reefs assume a linear functional relationship between the ambient seawater aragonite saturation state (Omega a) and net ecosystem calcification (NEC). We quantified NEC in a healthy coral reef lagoon in the Great Barrier Reef during different times of the day. Our observations revealed a diel hysteresis pattern in the NEC versus Omega a relationship, with peak NEC rates occurring before the Omega a peak and relatively steady nighttime NEC in spite of variable Omega a. Net ecosystem production had stronger correlations with NEC than light, temperature, nutrients, pH, and Omega a. The observed hysteresis may represent an overlooked challenge for predicting the effects of OA on coral reefs. If widespread, the hysteresis could prevent the use of a linear extrapolation to determine critical Omega a threshold levels required to shift coral reefs from a net calcifying to a net dissolving state.