Natural variation, and the capacity to adapt to ocean acidification in the keystone sea urchin Strongylocentrotus purpuratus

A rapidly growing body of literature documents the potential negative effects of CO₂-driven ocean acidification (OA) on marine organisms. However, nearly all of this work has focused on the effects of future conditions on modern populations, neglecting the role of adaptation. Rapid evolution can alter demographic responses to environmental change, ultimately affecting the likelihood of population persistence, but the capacity for adaptation will differ among populations and species. Here, we measure the capacity of the ecologically important purple sea urchin Strongylocentrotus purpuratus to adapt to OA, using a breeding experiment to estimate additive genetic variance for larval size (an important component of fitness) under future high pCO₂/low pH conditions. Although larvae reared under future conditions were smaller than those reared under present-day conditions, we show that there is also abundant genetic variation for body size under elevated pCO₂, indicating that this trait can evolve. The observed heritability of size was 0.40±0.32 (95% CI) under low pCO₂, and 0.50±0.30 under high pCO₂ conditions. Accounting for the observed genetic variation in models of future larval size and demographic rates substantially alters projections of performance for this species in the future ocean. Importantly, our model shows that after incorporating the effects of adaptation, the OA-driven decrease in population growth rate is up to 50% smaller, than that predicted by the “no-adaptation” scenario. Adults used in the experiment were collected from two sites on the coast of the Northeast Pacific that are characterized by different pH regimes, as measured by autonomous sensors. Comparing results between sites, we also found subtle differences in larval size under high pCO₂ rearing conditions, consistent with local adaptation to carbonate chemistry in the field. These results suggest that spatially varying selection may help to maintain genetic variation necessary for adaptation to future ocean acidification.

Fertilization success of an arctic sea urchin species, Strongylocentrotus droebachiensis (O. F. Müller, 1776) under CO2-induced ocean acidification

Sea urchins as broadcasting spawners, release their gametes into open water for fertilization, thus being particularly vulnerable to ocean acidification. In this study, we assessed the effects of different pH scenarios on fertilization success of Strongylocentrotus droebachiensis, collected at Spitsbergen, Arctic. We achieved acidification by bubbling CO₂ into filtered seawater using partial pressures (pCO₂) of 180, 380, 980, 1400 and 3000 μatm}. Untreated filtered seawater was used as control. We recorded fertilization rates and diagnosed morphological aberrations after post-fertilization periods of 1 h and 3 h under different exposure conditions in experiments with and without pre-incubation of the eggs prior to fertilization. In parallel, we conducted measurements of intracellular pH changes using BCECF/AM in unfertilized eggs exposed to a range of acidified seawater. We observed increasing rates of polyspermy in relation to higher seawater pCO₂, which might be due to failures in the formation of the fertilization envelope. In addition, our experiments showed anomalies in fertilized eggs: incomplete lifting-off of the fertilization envelope and blebs of the hyaline layer. Other drastic malformations consisted of constriction, extrusion, vacuolization or degeneration (observed as a gradient from the cortex to the central region of the cell) of the egg cytoplasm, and irregular cell divisions until 2- to 4-cell stages. The intracellular pH (pH_i) decreased significantly from 1400 μatm on. All results indicate a decreasing fertilization success at CO₂ concentrations from 1400 μatm upwards. Exposure time to low pH might be a threatening factor for the cellular buffer capacity, viability, and development after fertilization.

Effects of ocean acidification on growth and physiology of Ulva lactuca (Chlorophyta) in a rockpool-scenario

Rising atmospheric CO₂-concentrations will have severe consequences for a variety of biological processes. We investigated the responses of the green alga Ulva lactuca (Linnaeus) to rising CO₂-concentrations in a rockpool scenario. U. lactuca was cultured under aeration with air containing either preindustrial pCO₂ (280 μatm) or the pCO₂ predicted by the end of the 21st century (700 μatm) for 31 days. We addressed the following question: Will elevated CO₂-concentrations affect photosynthesis (net photosynthesis, maximum relative electron transport rate (rETR(max)), maximum quantum yield (Fv/Fm), pigment composition) and growth of U. lactuca in rockpools with limited water exchange? Two phases of the experiment were distinguished: In the initial phase (day 1–4) the Seawater Carbonate System (SWCS) of the culture medium could be adjusted to the selected atmospheric pCO₂ condition by continuous aeration with target pCO₂ values. In the second phase (day 4–31) the SWCS was largely determined by the metabolism of the growing U. lactuca biomass. In the initial phase, Fv/Fm and rETR(max) were only slightly elevated at high CO₂-concentrations, whereas growth was significantly enhanced. After 31 days the Chl a content of the thalli was significantly lower under future conditions and the photosynthesis of thalli grown under preindustrial conditions was not dependent on external carbonic anhydrase. Biomass increased significantly at high CO₂-concentrations. At low CO₂-concentrations most adult thalli disintegrated between day 14 and 21, whereas at high CO₂-concentrations most thalli remained integer until day 31. Thallus disintegration at low CO₂-concentrations was mirrored by a drastic decline in seawater dissolved inorganic carbon and HCO₃⁻. Accordingly, the SWCS differed significantly between the treatments. Our results indicated a slight enhancement of photosynthetic performance and significantly elevated growth of U. lactuca at future CO₂-concentrations. The accelerated thallus disintegration at high CO₂-concentrations under conditions of limited water exchange indicates additional CO₂ effects on the life cycle of U. lactuca when living in rockpools.

High risk of extinction of benthic foraminifera in this century due to ocean acidification

Increased atmospheric CO₂ concentrations lead to decreased pH and carbonate availability in the ocean (Ocean Acidification, OA). Carbon dioxide seeps serve as ‘windows into the future’ to study the ability of marine invertebrates to acclimatise to OA. We studied benthic foraminifera in sediments from shallow volcanic CO₂ seeps in Papua New Guinea. Conditions follow a gradient from present day pH/pCO₂ to those expected past 2100. We show that foraminiferal densities and diversity declined steeply with increasing pCO_2. Foraminifera were almost absent at sites with pH < 7.9 (>700 μatm pCO₂). Symbiont-bearing species did not exhibit reduced vulnerability to extinction at <7.9 pH. Non-calcifying taxa declined less steeply along pCO₂ gradients, but were also absent in samples at pH < 7.9. Data suggest the possibility of an OA induced ecological extinction of shallow tropical benthic foraminifera by 2100; similar to extinctions observed in the geological past.

Food availability and pCO2 impacts on planulation, juvenile survival, and calcification of the azooxanthellate scleractinian coral, Balanophyllia elegans

Ocean acidification, the assimilation of atmospheric CO₂ by the oceans that decreases the pH and CaCO₃ saturation state (Ω) of seawater, is projected to have severe consequences for calcifying organisms. Strong evidence suggests that tropical reef-building corals containing algal symbionts (zooxanthellae) will experience dramatic declines in calcification over the next century. The responses of azooxanthellate corals to ocean acidification are less well understood, and because they cannot obtain extra photosynthetic energy from symbionts, they provide a system for studying the direct effects of acidification on the energy available for calcification. The orange cup coral Balanophyllia elegans is a solitary, azooxanthellate scleractinian species common on the California coast where it thrives in the low pH waters of an upwelling regime. During an 8 month study, we addressed the effects of three pCO₂ treatments (410, 770, and 1230 μatm) and two feeding frequencies (High Food and Low Food) on adult Balanophyllia elegans planulation (larval release) rates, and on the survival, growth, and calcification of their juvenile offspring. Planulation rates were affected by food level but not pCO₂, while juvenile survival was highest under 410 μatm and High Food conditions. Our results suggest that feeding rate has a greater impact on calcification of B. elegans than pCO₂. Net calcification was positive even at 1230 μatm (~ 3 times current atmospheric pCO₂), although the increase from 410 to 1230 μatm reduced overall calcification by ~ 25–45%, and reduced skeletal density by ~ 35–45%. Higher pCO₂ also altered aragonite crystal morphology significantly. We discuss how feeding frequency affects azooxanthellate coral calcification, and how B. elegans may respond to ocean acidification in coastal upwelling waters.

Deformities in larvae and juvenile European lobster (Homarus gammarus) exposed to lower pH at two different temperatures

Trends of increasing temperatures and ocean acidification are expected to influence benthic marine resources, especially calcifying organisms. The European lobster (Homarus gammarus) is among those species at risk. A project was initiated in 2011 aiming to investigate long-term synergistic effects of temperature and projected increases in ocean acidification on the life cycle of lobster. Larvae were exposed to pCO₂ levels of ambient water (water intake at 90 m depth, tentatively of 380 μatm pCO₂), 727 and 1217 μatm pCO₂, at temperatures 10 and 18 °C. Long-term exposure lasted until 5 months of age. Thereafter the surviving juveniles were transferred to ambient water at 14 °C. At 18 °C the development from Stage 1 to 4 lasted from 14 to 16 days, as predicted under normal pH values. Growth was very slow at 10 °C and resulted in only two larvae reaching Stage 4 in the ambient treatment. There were no significant differences in carapace length at the various larval stages between the different treatments, but there were differences in total length and dry weight at Stage 1 at 10 °C, Stage 2 at both temperatures, producing larvae slightly larger in size and lighter by dry weight in the exposed treatments. Stage 3 larvae raised in 18 °C and 1217 μatm pCO₂ were also larger in size and heavier by dry weight compared with 727 μatm. Unfortunate circumstances precluded a full comparison across stages and treatment. Deformities were however observed in both larvae and juveniles. At 10 °C, about 20% of the larvae exposed to elevated pCO₂were deformed, compared with 0% in larvae raised in pH above 8.0. At 18 °C and in high pCO₂ treatment, 31.5% of the larvae were deformed. Occurrence of deformities after 5 months of exposure was 33 and 44% in juveniles raised in ambient and low pCO₂, respectively, and 20% in juveniles exposed to high pCO₂. Some of the deformities will possibly affect the ability to find food, sexual partner (walking legs, claw and antenna), respiration (carapace), and ability to swim (tail-fan damages).

Consumers mediate the effects of experimental ocean acidification and warming on primary producers

It is well known that ocean acidification can have profound impacts on marine organisms. However, we know little about the direct and indirect effects of ocean acidification and also how these effects interact with other features of environmental change such as warming and declining consumer pressure. In this study, we tested whether the presence of consumers (invertebrate mesograzers) influenced the interactive effects of ocean acidification and warming on benthic microalgae in a seagrass community mesocosm experiment. Net effects of acidification and warming on benthic microalgal biomass and production, as assessed by analysis of variance, were relatively weak regardless of grazer presence. However, partitioning these net effects into direct and indirect effects using structural equation modeling revealed several strong relationships. In the absence of grazers, benthic microalgae were negatively and indirectly affected by sediment-associated microalgal grazers and macroalgal shading, but directly and positively affected by acidification and warming. Combining indirect and direct effects yielded no or weak net effects. In the presence of grazers, almost all direct and indirect climate effects were nonsignificant. Our analyses highlight that (i) indirect effects of climate change may be at least as strong as direct effects, (ii) grazers are crucial in mediating these effects, and (iii) effects of ocean acidification may be apparent only through indirect effects and in combination with other variables (e.g., warming). These findings highlight the importance of experimental designs and statistical analyses that allow us to separate and quantify the direct and indirect effects of multiple climate variables on natural communities.

Potential acidification impacts on zooplankton in CCS leakage scenarios

Carbon capture and storage (CCS) technologies involve localized acidification of significant volumes of seawater, inhabited mainly by planktonic species. Knowledge on potential impacts of these techniques on the survival and physiology of zooplankton, and subsequent consequences for ecosystem health in targeted areas, is scarce. The recent literature has a focus on anthropogenic greenhouse gas emissions into the atmosphere, leading to enhanced absorption of CO₂ by the oceans and a lowered seawater pH, termed ocean acidification. These studies explore the effects of changes in seawater chemistry, as predicted by climate models for the end of this century, on marine biota. Early studies have used unrealistically severe CO₂/pH values in this context, but are relevant for CCS leakage scenarios. Little studied meso- and bathypelagic species of the deep sea may be especially vulnerable, as well as vertically migrating zooplankton, which require significant residence times at great depths as part of their life cycle.

Effects of ocean acidification on the larval growth of olive flounder (Paralichthys olivaceus)

Little is known about how marine fishes respond to the reduced pH condition caused by the increased CO₂ in the atmosphere. We investigated the effects of CO₂ concentration on the growth of olive flounder (Paralichthys olivaceus) larvae. Newly hatched larvae were reared in three different concentrations of CO₂ (574, 988 and 1297 μatm CO₂) in temperature-controlled water tanks until metamorphosis (4 weeks). Body lengths, weights, and the concentration of some chemical elements in larval tissue were measured at the completion of each experiment, and experiment was repeated three times in May, June, and July 2011. Results indicated that body length and weight of flounder larvae were significantly increased with increasing CO₂ concentration (P < 0.05). Daily growth rates of flounder larvae were higher (0.391 mm) from the high CO₂ concentration (1297 μatm) than those (0.361 mm and 0.360 mm) from the lower ones (988 and 574 μatm).The measurement on some chemical elements (Ca, Fe, Cu, Zn and Sr) in fish tissue also revealed the increasing tendency of element concentration with increasing CO₂ in seawater, although statistical significance cannot be tested due to the single measurement. It suggests that there are enrichment processes of these cations in larval tissue in the low pH condition.

Effects of sub-lethal CO2(aq) concentrations on the performance of intensively reared gilthead seabream (Sparus aurata) in brackish water: flow-through experiments and full-scale RAS results

The effects sub-lethal CO_2(aq) concentrations were tested for the first time on gilthead seabream (Sparus aurata) juveniles (4 to 25 g; 64 growth days) and adult (∼300-400 g; 71 days) fish, both in fully controlled pilot tests and the latter also as part of full-scale RAS (recirculating aquaculture system) operation. In the pilot experiments (concentration range 5.2 to 56.3 mgCO₂/L) the specific growth rate, mortality rate, and physical fish disorders were monitored. In the full scale experiment, two groups of fish, originally from the same batch, were exposed for 197 days to controlled (by NaOH dosage) and uncontrolled pH conditions, resulting in exposure of the fish to significantly different CO_2(aq) concentrations. The pilot results showed, as expected, that the seabream fish grew faster at the lower CO₂ concentrations and that the growth rate of both juveniles and adult fish was only minimally inhibited up to roughly 20 mg CO₂/L (compared to a previously published curve). Mortality rate was considerable only at the highest CO₂ concentration (∼56 mgCO₂/L). Physical irregularities were not observed, apart from abnormally-high absence of swim bladder at the highest CO_2(aq) treatment. The (statistically significant) results from the full-scale RAS operation showed that growing gilthead seabream for 197 days at roughly constant and relatively low (∼16 mg/L) CO_2(aq) concentration resulted in fish with ∼10% larger mean weight relative to the fish grown in ponds in which CO_2(aq) was not controlled and its concentration fluctuated daily between 19 and 37 mg/L.