Maintained larval growth in mussel larvae exposed to acidified undersaturated seawater

Ocean acidification (OA) is known to affect bivalve early life-stages. We tested responses of blue mussel larvae to a wide range of pH in order to identify their tolerance threshold. Our results confirmed that decreasing seawater pH and decreasing saturation state increases larval mortality rate and the percentage of abnormally developing larvae. Virtually no larvae reared at average pHT 7.16 were able to feed or reach the D-shell stage and their development appeared to be arrested at the trochophore stage. However larvae were capable of reaching the D-shell stage under milder acidification (pHT=7.35, 7.6, 7.85) including in under-saturated seawater with omega Aragonite as low as 0.54±0.01 (mean±s. e. m.), with a tipping point for normal development identified at pHT 7.765. Additionally growth rate of normally developing larvae was not affected by lower pHT despite potential increased energy costs associated with compensatory calcification in response to increased shell dissolution. Overall, our results on OA impacts on mussel larvae suggest an average pHT of 7.16 is beyond their physiological tolerance threshold and indicate a shift in energy allocation towards growth in some individuals revealing potential OA resilience.

Seawater carbonate chemistry and biometry and dissolution features of the benthic foraminifer Ammonia aomoriensis in a laboratory experiment

Culturing experiments were performed with the benthic foraminifer Ammonia aomoriensis from Flensburg Fjord, western Baltic Sea. The experiments simulated a projected rise in atmospheric CO2 concentrations. We exposed specimens to 5 seawater pCO2 levels ranging from 618 µatm (pH 7.9) to 3130 µatm (pH 7.2) for 6 wk. Growth rates and mortality differed significantly among pCO2 treatments. The highest increase of mean test diameter (19%) was observed at 618 µatm. At partial pressures >1829 µatm, the mean test diameter was observed to decrease, by up to 22% at 3130 µatm. At pCO2 levels of 618 and 751 µatm, A. aomoriensis tests were found intact after the experiment. The outer chambers of specimens incubated at 929 and 1829 µatm were severely damaged by corrosion. Visual inspection of specimens incubated at 3130 µatm revealed wall dissolution of all outer chambers, only their inner organic lining stayed intact. Our results demonstrate that pCO2 values of >=929 µatm in Baltic Sea waters cause reduced growth of A. aomoriensis and lead to shell dissolution. The bottom waters in Flensburg Fjord and adjacent areas regularly experience pCO2 levels in this range during summer and fall. Increasing atmospheric CO2 concentrations are likely to extend and intensify these periods of undersaturation. This may eventually slow down calcification in A. aomoriensis to the extent that net carbonate precipitation terminates. The possible disappearance of this species from the Baltic Sea and other areas prone to seasonal undersaturation would likely cause significant shifts in shallow-water benthic ecosystems in the near future.

Seawater carbonate chemistry and growth rate of Emiliania huxleyi in lab experiment

Predicting the impacts of environmental change on marine organisms, food webs, and biogeochemical cycles presently relies almost exclusively on short-term physiological studies, while the possibility of adaptive evolution is often ignored. Here, we assess adaptive evolution in the coccolithophore Emiliania huxleyi, a well-established model species in biological oceanography, in response to ocean acidification. We previously demonstrated that this globally important marine phytoplankton species adapts within 500 generations to elevated CO2. After 750 and 1000 generations, no further fitness increase occurred, and we observed phenotypic convergence between replicate populations. We then exposed adapted populations to two novel environments to investigate whether or not the underlying basis for high CO2-adaptation involves functional genetic divergence, assuming that different novel mutations become apparent via divergent pleiotropic effects. The novel environment "high light" did not reveal such genetic divergence whereas growth in a low-salinity environment revealed strong pleiotropic effects in high CO2 adapted populations, indicating divergent genetic bases for adaptation to high CO2. This suggests that pleiotropy plays an important role in adaptation of natural E. huxleyi populations to ocean acidification. Our study highlights the potential mutual benefits for oceanography and evolutionary biology of using ecologically important marine phytoplankton for microbial evolution experiments.

Physiological energetics of the thick shell mussel Mytilus coruscus exposed to seawater acidification and thermal stress

Anthropogenic CO2 emissions have caused seawater temperature elevation and ocean acidification. In view of both phenomena are occurring simultaneously, their combined effects on marine species must be experimentally evaluated. The purpose of this study was to estimate the combined effects of seawater acidification and temperature increase on the energy budget of the thick shell mussel Mytilus coruscus. Juvenile mussels were exposed to six combined treatments with three pH levels (8.1, 7.7 and 7.3) * two temperatures (25 °C and 30 °C) for 14 d. We found that clearance rates (CRs), food absorption efficiencies (AEs), respiration rates (RRs), ammonium excretion rates (ER), scope for growth (SFG) and O:N ratios were significantly reduced by elevated temperature sometimes during the whole experiments. Low pH showed significant negative effects on RR and ER, and significantly increased O:N ratios, but showed almost no effects on CR, AE and SFG of M. coruscus. Nevertheless, their interactive effects were observed in RR, ER and O:N ratios. PCA revealed positive relationships among most physiological indicators, especially between SFG and CR under normal temperatures compared to high temperatures. PCA also showed that the high RR was closely correlated to an increasing ER with increasing pH levels. These results suggest that physiological energetics of juvenile M. coruscus are able to acclimate to CO2 acidification with a little physiological effect, but not increased temperatures. Therefore, the negative effects of a temperature increase could potentially impact the ecophysiological responses of M. coruscus and have significant ecological consequences, mainly in those habitats where this species is dominant in terms of abundance and biomass.

Echinometra sea urchins acclimatised to elevated pCO2 at volcanic vents outperform those under present-day pCO2 conditions

Rising atmospheric CO2 concentrations will significantly reduce ocean pH during the 21st century (ocean acidification, OA). This may hamper calcification in marine organisms such as corals and echinoderms, as shown in many laboratory-based experiments. Sea urchins are considered highly vulnerable to OA. We studied an Echinometra species on natural volcanic CO2 vents in Papua New Guinea, where they are CO2-acclimatized and also subjected to secondary ecological changes from elevated CO2. Near the vent site, the urchins experienced large daily variations in pH (> 1 unit) and pCO2 (> 2000 ppm) and average pH values (pHT 7.73) much below those expected under the most pessimistic future emission scenarios. Growth was measured over a 17-month period using tetracycline tagging of the calcareous feeding lanterns. Average-sized urchins grew more than twice as fast at the vent compared with those at an adjacent control site, and assumed larger sizes at the vent compared to the control site and two other sites at another reef near-by. A small reduction in gonad weight was detected at the vents, but no differences in mortality, respiration, or degree of test calcification were detected between urchins from vent and control populations. Thus, urchins did not only persist but actually 'thrived' under extreme CO2 conditions. We suggest an ecological basis for this response: increased algal productivity under increased pCO2 provided more food at the vent, resulting in higher growth rates. The wider implication of our observation is that laboratory studies on non-acclimatized specimens, which typically do not consider ecological changes, can lead to erroneous conclusions on responses to global change.

Synergistic effects of ocean acidification and warming on overwintering pteropods in the Arctic

Ocean acidification and warming will be most pronounced in the Arctic Ocean. Aragonite shell-bearing pteropods in the Arctic are expected to be among the first species to suffer from ocean acidification. Carbonate undersaturation in the Arctic will first occur in winter and because this period is also characterized by low food availability, the overwintering stages of polar pteropods may develop into a bottleneck in their life cycle. The impacts of ocean acidification and warming on growth, shell degradation (dissolution), and mortality of two thecosome pteropods, the polar Limacina helicina and the boreal L. retroversa, were studied for the first time during the Arctic winter in the Kongsfjord (Svalbard). The abundance of L. helicina and L. retroversa varied from 23.5 to 120 ind /m2 and 12 to 38 ind /m2, and the mean shell size ranged from 920 to 981 µm and 810 to 823 µm, respectively. Seawater was aragonite-undersaturated at the overwintering depths of pteropods on two out of ten days of our observations. A 7-day experiment [temperature levels: 2 and 7 °C, pCO2 levels: 350, 650 (only for L. helicina) and 880 ?atm] revealed a significant pCO2 effect on shell degradation in both species, and synergistic effects between temperature and pCO2 for L. helicina. A comparison of live and dead specimens kept under the same experimental conditions indicated that both species were capable of actively reducing the impacts of acidification on shell dissolution. A higher vulnerability to increasing pCO2 and temperature during the winter season is indicated compared with a similar study from fall 2009. Considering the species winter phenology and the seasonal changes in carbonate chemistry in Arctic waters, negative climate change effects on Arctic thecosomes are likely to show up first during winter, possibly well before ocean acidification effects become detectable during the summer season.

Rising CO2 and increased light exposure synergistically reduce marine primary productivity

Carbon dioxide and light are two major prerequisites of photosynthesis. Rising CO2 levels in oceanic surface waters in combination with ample light supply are therefore often considered stimulatory to marine primary production. Here we show that the combination of an increase in both CO2 and light exposure negatively impacts photosynthesis and growth of marine primary producers. When exposed to CO2 concentrations projected for the end of this century, natural phytoplankton assemblages of the South China Sea responded with decreased primary production and increased light stress at light intensities representative of the upper surface layer. The phytoplankton community shifted away from diatoms, the dominant phytoplankton group during our field campaigns. To examine the underlying mechanisms of the observed responses, we grew diatoms at different CO2 concentrations and under varying levels (5-100%) of solar radiation experienced by the phytoplankton at different depths of the euphotic zone. Above 22-36% of incident surface irradiance, growth rates in the high-CO2-grown cells were inversely related to light levels and exhibited reduced thresholds at which light becomes inhibitory. Future shoaling of upper-mixed-layer depths will expose phytoplankton to increased mean light intensities. In combination with rising CO2 levels, this may cause a widespread decline in marine primary production and a community shift away from diatoms, the main algal group that supports higher trophic levels and carbon export in the ocean.

Adaptive evolution of a key phytoplankton species to ocean acidification

Ocean acidification, the drop in seawater pH associated with the ongoing enrichment of marine waters with carbon dioxide from fossil fuel burning, may seriously impair marine calcifying organisms. Our present understanding of the sensitivity of marine life to ocean acidification is based primarily on short-term experiments, in which organisms are exposed to increased concentrations of CO2. However, phytoplankton species with short generation times, in particular, may be able to respond to environmental alterations through adaptive evolution. Here, we examine the ability of the world's single most important calcifying organism, the coccolithophore Emiliania huxleyi, to evolve in response to ocean acidification in two 500-generation selection experiments. Specifically, we exposed E. huxleyi populations founded by single or multiple clones to increased concentrations of CO2. Around 500 asexual generations later we assessed their fitness. Compared with populations kept at ambient CO2 partial pressure, those selected at increased partial pressure exhibited higher growth rates, in both the single- and multiclone experiment, when tested under ocean acidification conditions. Calcification was partly restored: rates were lower under increased CO2 conditions in all cultures, but were up to 50% higher in adapted compared with non-adapted cultures. We suggest that contemporary evolution could help to maintain the functionality of microbial processes at the base of marine food webs in the face of global change.

Seawater carbonate chemistry and skeletal development, size, weight, total lipid and symbiont density of coral Favia fragum in a laboratory experiment

Ocean acidification (OA) threatens the existence of coral reefs by slowing the rate of calcium carbonate (CaCO3) production of framework-building corals thus reducing the amount of CaCO3 the reef can produce to counteract natural dissolution. Some evidence exists to suggest that elevated levels of dissolved inorganic nutrients can reduce the impact of OA on coral calcification. Here, we investigated the potential for enhanced energetic status of juvenile corals, achieved via heterotrophic feeding, to modulate the negative impact of OA on calcification. Larvae of the common Atlantic golf ball coral, Favia fragum, were collected and reared for 3 weeks under ambient (421 µatm) or significantly elevated (1,311 µatm) CO2 conditions. The metamorphosed, zooxanthellate spat were either fed brine shrimp (i.e., received nutrition from photosynthesis plus heterotrophy) or not fed (i.e., primarily autotrophic). Regardless of CO2 condition, the skeletons of fed corals exhibited accelerated development of septal cycles and were larger than those of unfed corals. At each CO2 level, fed corals accreted more CaCO3 than unfed corals, and fed corals reared under 1,311 µatm CO2 accreted as much CaCO3 as unfed corals reared under ambient CO2. However, feeding did not alter the sensitivity of calcification to increased CO2; Delta calcification/Delta Omega was comparable for fed and unfed corals. Our results suggest that calcification rates of nutritionally replete juvenile corals will decline as OA intensifies over the course of this century. Critically, however, such corals could maintain higher rates of skeletal growth and CaCO3 production under OA than those in nutritionally limited environments.

Effects of ocean acidification on embryonic respiration and development of a temperate wrasse living along a natural CO2 gradient

Volcanic CO2 seeps provide opportunities to investigate the effects of ocean acidification on organisms in the wild. To understand the influence of increasing CO2 concentrations on the metabolic rate (oxygen consumption) and the development of ocellated wrasse early life stages, we ran two field experiments, collecting embryos from nesting sites with different partial pressures of CO2 [pCO2; ambient (400 µatm) and high (800-1000 µatm)] and reciprocally transplanting embryos from ambient- to high-CO2 sites for 30 h. Ocellated wrasse offspring brooded in different CO2 conditions had similar responses, but after transplanting portions of nests to the high-CO2 site, embryos from parents that spawned in ambient conditions had higher metabolic rates. Although metabolic phenotypic plasticity may show a positive response to high CO2, it often comes at a cost, in this case as a smaller size at hatching. This can have adverse effects because smaller larvae often exhibit a lower survival in the wild. However, the adverse effects of increased CO2 on metabolism and development did not occur when embryos from the high-CO2 nesting site were exposed to ambient conditions, suggesting that offspring from the high-CO2 nesting site could be resilient to a wider range of pCO2 values than those belonging to the site with present-day pCO2 levels. Our study identifies a crucial need to increase the number of studies dealing with these processes under global change trajectories and to expand these to naturally high-CO2 environments, in order to assess further the adaptive plasticity mechanism that encompasses non-genetic inheritance (epigenetics) through parental exposure and other downstream consequences, such as survival of larvae.

Effect of ocean warming and acidification on the early life stages of subtropical Acropora spicifera

This study investigated the impacts of acidified seawater (pCO2 900 µatm) and elevated water temperature (+3 °C) on the early life history stages of Acropora spicifera from the subtropical Houtman Abrolhos Islands (28°S) in Western Australia. Settlement rates were unaffected by high temperature (27 °C, 250 µatm), high pCO2 (24 °C, 900 µatm), or a combination of both high temperature and high pCO2 treatments (27 °C, 900 µatm). There were also no significant differences in rates of post-settlement survival after 4 weeks of exposure between any of the treatments, with survival ranging from 60 to 70 % regardless of treatment. Similarly, calcification, as determined by the skeletal weight of recruits, was unaffected by an increase in water temperature under both ambient and high pCO2 conditions. In contrast, high pCO2 significantly reduced early skeletal development, with mean skeletal weight in the high pCO2 and combined treatments reduced by 60 and 48 %, respectively, compared to control weights. Elevated temperature appeared to have a partially mitigative effect on calcification under high pCO2; however, this effect was not significant. Our results show that rates of settlement, post-settlement survival, and calcification in subtropical corals are relatively resilient to increases in temperature. This is in marked contrast to the sensitivity to temperature reported for the majority of tropical larvae and recruits in the literature. The subtropical corals in this study appear able to withstand an increase in temperature of 3 °C above ambient, indicating that they may have a wider thermal tolerance range and may not be adversely affected by initial increases in water temperature from subtropical 24 to 27 °C. However, the reduction in skeletal weight with high pCO2 indicates that early skeletal formation will be highly vulnerable to the changes in ocean pCO2 expected to occur over the twenty-first century, with implications for their longer-term growth and resilience.

Evaluation of the threat of marine CO2 leakage-associated acidification on the toxicity of sediment metals to juvenile bivalves

The effects of the acidification associated with CO2 leakage from sub-seabed geological storage was studied by the evaluation of the short-term effects of CO2-induced acidification on juveniles of the bivalve Ruditapes philippinarum. Laboratory scale experiments were performed using a CO2-bubbling system designed to conduct ecotoxicological assays. The organisms were exposed for 10 days to elutriates of sediments collected in different littoral areas that were subjected to various pH treatments (pH 7.1; pH 6.6; pH 6.1). The acute pH-associated effects on the bivalves were observed, and the dissolved metals in the elutriates were measured. The median toxic effect pH was calculated, which ranged from 6.33 and 6.45. The amount of dissolved Zn in the sediment elutriates increased in parallel with the pH reductions and was correlated with the proton concentrations. The pH, the pCO2 and the dissolved metal concentrations (Zn and Fe) were linked with the mortality of the exposed bivalves.

Colony-specific calcification and mortality under ocean acidification in the branching coral Montipora digitata

Ocean acidification (OA) threatens calcifying marine organisms including reef-building corals. In this study, we examined the OA responses of individual colonies of the branching scleractinian coral Montipora digitata. We exposed nubbins of unique colonies (n = 15) to ambient or elevated pCO2 under natural light and temperature regimes for 110 days. Although elevated pCO2 exposure on average reduced calcification, individual colonies showed unique responses ranging from declines in positive calcification to negative calcification (decalcification) to no change. Similarly, mortality was greater on average in elevated pCO2, but also showed colony-specific patterns. High variation in colony responses suggests the possibility that ongoing OA may lead to natural selection of OA-tolerant colonies within a coral population.

Seawater carbonate chemistry and calcification in the tropical urchin Echinometra viridis in a laboratory experiment

Atmospheric carbon dioxide (pCO2) has risen from approximately 280 to 400 ppm since the Industrial Revolution, due mainly to the combustion of fossil fuels, deforestation, and cement production. It is predicted to reach as high as 900 ppm by the end of this century. Ocean acidification resulting from the release of anthropogenic CO2 has been shown to impair the ability of some marine calcifiers to build their shells and skeletons. Here, we present the results of ocean acidification experiments designed to assess the effects of an increase in atmospheric pCO2 from ca. 448 to 827 ppm on calcification rates of the tropical urchin Echinometra viridis. Experiments were conducted under the urchin's winter (20 °C) and summer (30 °C) water temperatures in order to identify seasonal differences in the urchin's response to ocean acidification. The experiments reveal that calcification rates decreased for urchins reared under elevated pCO2, with the decline being more pronounced under wintertime temperatures than under summertime temperatures. These results indicate that the urchin E. viridis will be negatively impacted by CO2-induced ocean acidification that is predicted to occur by the end of this century. These results also suggest that impact of CO2-induced ocean acidification on urchin calcification will be more severe in the winter and in cooler waters.