Food availability outweighs ocean acidification effects in juvenile Mytilus edulis: laboratory and field experiments

Ocean acidification has the potential to affect growth and calcification of benthic marine invertebrates, particularly during their early life history. We exposed field-collected juveniles of Asterias rubens from Kiel Fjord (western Baltic Sea) to 3 seawater CO2 partial pressure (pCO2) levels (ranging from around 650 to 3500 µatm) in a long-term (39 wk) and a short-term (6 wk) experiment. In both experiments, survival and calcification were not affected by elevated pCO2. However, feeding rates decreased strongly with increasing pCO2, while aerobic metabolism and NH4+ excretion were not significantly affected by CO2 exposure. Consequently, high pCO2 reduced the scope for growth in A. rubens. Growth rates decreased substantially with increasing pCO2 and were reduced even at pCO2 levels occurring in the habitat today (e.g. during upwelling events). Sea stars were not able to acclimate to higher pCO2, and growth performance did not recover during the long-term experiment. Therefore, the top-down control exerted by this keystone species may be diminished during periods of high environmental pCO2 that already occur occasionally and will be even higher in the future. However, some individuals were able to grow at high rates even at high pCO2, indicating potential for rapid adaption. The selection of adapted specimens of A. rubens in this seasonally acidified habitat may lead to higher CO2 tolerance in adult sea stars of this population compared to the juvenile stage. Future studies need to address the synergistic effects of multiple stressors such as acidification, warming and reduced salinity, which will simultaneously impact the performance of sea stars in this habitat.

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.

Abstract. CO2 emissions are leading to an acidification of the oceans. Predicting marine community vulnerability towards acidification is difficult, as adaptation processes cannot be accounted for in most experimental studies. Naturally CO2 enriched sites thus can serve as valuable proxies for future changes in community structure. Here we describe a natural analogue site in the Western Baltic Sea. Seawater pCO2 in Kiel Fjord is elevated for large parts of the year due to upwelling of CO2 rich waters. Peak pCO2 values of >230 Pa (>2300 μatm) and pHNBS values of <7.5 are encountered during summer and autumn, average pCO2 values are ~70 Pa (~700 μatm). In contrast to previously described naturally CO2 enriched sites that have suggested a progressive displacement of calcifying auto- and heterotrophic species, the macrobenthic community in Kiel Fjord is dominated by calcifying invertebrates. We show that blue mussels from Kiel Fjord can maintain control rates of somatic and shell growth at a pCO2 of 142 Pa (1400 μatm, pHNBS = 7.7). Juvenile mussel recruitment peaks during the summer months, when high water pCO2 values of ~100 Pa (~1000 μatm) prevail. Our findings indicate that calcifying keystone species may be able to cope with surface ocean pHNBS values projected for the end of this century when food supply is sufficient. However, owing to non-linear synergistic effects of future acidification and upwelling of corrosive water, peak seawater pCO2 in Kiel Fjord and many other productive estuarine habitats could increase to values >400 Pa (>4000 μatm). These changes will most likely affect calcification and recruitment, and increase external shell dissolution.

Polar oceans are predicted to be the first marine environments affected by ocean acidification (OA). Thysanoessa inermis is one of the most abundant krill species in northern waters of the Atlantic and a key species in the food web of this ecosystem. Yet, we know very little about potential OA effects on this species. We studied the effects of elevated pCO2 on T. inermis in a laboratory experiment by exposing individuals for 11 weeks to low and high pCO2 (450 and 1200 µatm, respectively, n = 12 per pCO2 treatment). Survival, growth, and moulting frequency was monitored during the experiment, and feeding and oxygen consumption rates (n = 3–5 per pCO2 treatment) were measured at the end of the experiment. No significant effects of high pCO2 on survival, growth, moulting, oxygen consumption, and feeding rate were observed, indicating that T. inermis is tolerant to predicted high OA levels. We also explored physical and chemical properties of waters near the collection area of krill, Rijpfjorden (Svalbard 80° North) during the polar summer (July–August). In situ measurements showed large temperature and salinity gradients from surface to bottom and pCO2 and pH ranged, respectively, 161–417 µatm and 7.99–8.37. Even though substantial spatial variability in pCO2 could be observed, krill in this area is not confronted yet with the investigated high pCO2 levels.

Understanding how rising seawater pCO2 and temperatures impact coral aragonite accretion is essential for predicting the future of reef ecosystems. Here, we report 2 long-term (10–11 month) studies assessing the effects of temperature (25 and 28 °C) and both high and low seawater pCO2 (180–750 μatm) on the calcification, photosynthesis and respiration of individual massive Porites spp. genotypes. Calcification rates were highly variable between genotypes, but high seawater pCO2 reduced calcification significantly in 4 of 7 genotypes cultured at 25 °C but in only 1 of 4 genotypes cultured at 28 °C. Increasing seawater temperature enhanced calcification in almost all corals, but the magnitude of this effect was seawater pCO2 dependent. The 3 °C temperature increase enhanced calcification rate on average by 3% at 180 μatm, by 35% at 260 μatm and by > 300% at 750 μatm. The rate increase at high seawater pCO2 exceeds that observed in inorganic aragonites. Responses of gross/net photosynthesis and respiration to temperature and seawater pCO2 varied between genotypes, but rates of all these processes were reduced at the higher seawater temperature. Increases in seawater temperature, below the thermal stress threshold, may mitigate against ocean acidification in this coral genus, but this moderation is not mediated by an increase in net photosynthesis. The response of coral calcification to temperature cannot be explained by symbiont productivity or by thermodynamic and kinetic influences on aragonite formation.

Increased maintenance costs at cellular, and consequently organism level, are thought to be involved in shaping the sensitivity of marine calcifiers to ocean acidification (OA). Yet, knowledge of the capacity of marine calcifiers to undergo metabolic adaptation is sparse. In Kiel Fjord, blue mussels thrive despite periodically high seawater PCO2, making this population interesting for studying metabolic adaptation under OA. Consequently, we conducted a multi-generation experiment and compared physiological responses of F1 mussels from 'tolerant' and 'sensitive' families exposed to OA for 1year. Family classifications were based on larval survival; tolerant families settled at all PCO2 levels (700, 1120, 2400µatm) while sensitive families did not settle at the highest PCO2 (≥99.8% mortality). We found similar filtration rates between family types at the control and intermediate PCO2 level. However, at 2400µatm, filtration and metabolic scope of gill tissue decreased in tolerant families, indicating functional limitations at the tissue level. Routine metabolic rates (RMR) and summed tissue respiration (gill and outer mantle tissue) of tolerant families were increased at intermediate PCO2, indicating elevated cellular homeostatic costs in various tissues. By contrast, OA did not affect tissue and routine metabolism of sensitive families. However, tolerant mussels were characterised by lower RMR at control PCO2 than sensitive families, which had variable RMR. This might provide the energetic scope to cover increased energetic demands under OA, highlighting the importance of analysing intra-population variability. The mechanisms shaping such difference in RMR and scope, and thus species' adaptation potential, remain to be identified.

Bivalve shell formation in a naturally CO2-enriched habitat: Unraveling the resilience mechanisms from elemental signatures

The effect of ocean acidification on tropical coral calcification: Insights from calcification fluid DIC chemistry

Ocean acidification has direct physiological effects on organisms, for example by dissolving the calcium carbonate structures of calcifying species. However, non-calcifiers may also be affected by changes in seawater chemistry. To disentangle the direct and indirect effects of ocean acidification on zooplankton growth, we undertook a study with two model organisms. Specifically, we investigated the individual effects of short-term exposure to high and low seawater pCO2, and different phytoplankton qualities as a result of different CO2 incubations on the growth of a heterotrophic dinoflagellate (Oxyrrhis marina) and a copepod species (Acartia tonsa). It was observed previously that higher CO2 concentrations can decrease phytoplankton food quality in terms of carbon : nutrient ratios. We therefore expected both seawater pCO2 (pH) and phytoplankton quality to result in decreased zooplankton growth. Although we expected lowest growth rates for all zooplankton under high seawater pCO2 and low algal quality, we found that direct pH effects on consumers seem to be of lesser importance than the associated decrease in algal quality. The decrease in the quality of primary producers under high pCO2 conditions negatively affected zooplankton growth, which may lead to lower availability of food for the next trophic level and thus potentially affect the recruitment of higher trophic levels.

Effects of ocean warming and acidification, combined with nutrient enrichment, on chemical composition and functional properties of Ulva rigida

Effects of temperature and pCO2 on lipid use and biological parameters of planulae of Pocillopora damicornis

There is concern that the increasing pCO2 following the Industrial Revolution Period might lead to ocean acidification, which could affect calcifying organisms in the oceans. Recently, negative emission technology has been attracting attention as an effective countermeasure for greenhouse gas emissions. In the ocean, ocean alkalinization technology is proposed to neutralize acidified oceans and enhance the absorption capacity of CO2 in the oceans. The potential effectiveness of ocean alkalinization technology is also suggested by the history of the Earth. During the Cretaceous period, when pCO2 is interpreted >1,000 ppm, calcifying organisms thrived in the Cretaceous oceans. It is hypothesized that it was due to the total alkalinity (TA) of the seawater being maintained higher, thereby kept the calcium carbonate saturation state at necessary. In this study, we examined this hypothesis as well as attempted to predict the effects of the application of current alkalinization techniques in the ocean on calcifying organisms.Clonal populations of large benthic foraminifers were cultured in highly alkalinized seawater under high pCO2 conditions, and amounts of calcification (weight and volume) were measured (Group 1: high TA and high pCO2). Specimens taken from same clonal population were kept in modern surface seawater (Group 2: low TA and low pCO2) as a control treatment. The same experiments were also conducted as Group 3 (low TA and high pCO2) to simulate future ocean acidification conditions, and as Group 4 (high TA and low pCO2) to simulate alkalinized ocean under a low pCO2 environment. It was showed significant differences in the amount of calcification in each of the Groups after three months cultivation. The amount of calcification in Group 1 was almost the same as that in the control treatment, confirming the possibility of maintaining the growth of calcifying organisms by alkalinization. Calcification amount in Group 3 was the smallest among all groups, indicating that future ocean acidification may inhibit calcification of large benthic foraminifers. In addition, the calcification rate was the greatest in Group 4, it is indicated that ocean alkalinization may enhance the calcification of the organisms. Finally, these results suggest that the calcium carbonate saturation state of seawater is an important parameter for calcification.

Ocean acidification alters the dissolved inorganic carbon chemistry of seawater and can reduce the calcification rates of tropical corals. Here we explore the effect of altering seawater pCO2 on the skeletal morphology of 4 genotypes of massive Porites spp. which display widely different calcification rates. Increasing seawater pCO2 causes significant changes in in the skeletal morphology of all Porites spp. studied regardless of whether or not calcification was significantly affected by seawater pCO2. Both the median calyx size and the proportion of skeletal surface occupied by the calices decreased significantly at 750 µatm compared to 400 µatm indicating that polyp size shrinks in this genus in response to ocean acidification. The coenosteum, connecting calices, expands to occupy a larger proportion of the coral surface to compensate for this decrease in calyx area. At high seawater pCO2 the spines deposited at the skeletal surface became more numerous and the trabeculae (vertical skeletal pillars) became significantly thinner in 2 of the 4 genotypes. The effect of high seawater pCO2 is most pronounced in the fastest growing coral and the regular placement of trabeculae and synapticulae is disturbed in this genotype resulting in a skeleton that is more randomly organised. The study demonstrates that ocean acidification decreases the polyp size and fundamentally alters the architecture of the skeleton in this major reef building species from the Indo-Pacific Ocean.

Mytilus edulis were cultured for 3 months under six different seawater pCO2 levels ranging from 380 to 4000 μatm. Specimen were taken from Kiel Fjord (Western Baltic Sea, Germany) which is a habitat with high and variable seawater pCO2 and related shifts in carbonate system speciation (e.g., low pH and low CaCO3 saturation state). Hemolymph (HL) and extrapallial fluid (EPF) samples were analyzed for pH and total dissolved inorganic carbon (CT) to calculate pCO2 and [HCO3−]. A second experiment was conducted for 2 months with three different pCO2 levels (380, 1400 and 4000 μatm). Boron isotopes (δ11B) were investigated by LA‐MC‐ICP‐MS (Laser Ablation–Multicollector–Inductively Coupled Plasma–Mass Spectrometry) in shell portions precipitated during experimental treatment time. Additionally, elemental ratios (B/Ca, Mg/Ca and Sr/Ca) in the EPF of specimen from the second experiment were measured via ICP‐OES (Inductively Coupled Plasma–Optical Emission Spectrometry). Extracellular pH was not significantly different in HL and EPF but systematically lower than ambient water pH. This is due to high extracellular pCO2 values, a prerequisite for metabolic CO2 excretion. No accumulation of extracellular [HCO3−] was measured. Elemental ratios (B/Ca, Mg/Ca and Sr/Ca) in the EPF increased slightly with pH which is in accordance with increasing growth and calcification rates at higher seawater pH values. Boron isotope ratios were highly variable between different individuals but also within single shells. This corresponds to a high individual variability in fluid B/Ca ratios and may be due to high boron concentrations in the organic parts of the shell. The mean δ11B value shows no trend with pH but appears to represent internal pH (EPF) rather than ambient water pH.

Eutrophic coastal regions are highly productive and greatly influenced by human activities. Primary production supporting the coastal ecosystems is supposed to be affected by progressive ocean acidification driven by increasing CO2 emissions. In order to investigate the effects of high pCO2 (HC) on eutrophic plankton community structure and ecological functions, we employed 9 mesocosms and carried out an experiment under ambient (∼410 ppmv) and future high (1000 ppmv) atmospheric pCO2 conditions, using in situ plankton community in Wuyuan Bay, East China Sea. Our results showed that HC along with natural seawater temperature rise significantly boosted biomass of diatoms with decreased abundance of dinoflagellates in the late stage of the experiment, demonstrating that HC repressed the succession from diatoms to dinoflagellates, a phenomenon observed during algal blooms in the East China Sea. HC did not significantly influence the primary production or biogenic silica contents of the phytoplankton assemblages. However, the HC treatments increased the abundance of viruses and heterotrophic bacteria, reflecting a refueling of nutrients for phytoplankton growth from virus-mediated cell lysis and bacterial degradation of organic matters. Conclusively, our results suggest that increasing CO2 concentrations can modulate plankton structure including the succession of phytoplankton community and the abundance of viruses and bacteria in eutrophic coastal waters, which may lead to altered biogeochemical cycles of carbon and nutrients.