Seawater carbonate chemistry and larval growth response of the Portuguese oyster (Crassostrea angulata) in a laboratory experiment

Rising anthropogenic carbon dioxide (CO2) dissolving into coastal waters is decreasing the pH and carbonate ion concentration, thereby lowering the saturation state of calcium carbonate (CaCO3) minerals through a process named ocean acidification (OA). The unprecedented threats posed by such low pH on calcifying larvae of several edible oyster species have not yet been fully explored. Effects of low pH (7.9, 7.6, 7.4) on the early growth phase of Portuguese oyster (Crassostrea angulata) veliger larvae was examined at ambient salinity (34 ppt) and the low-salinity (27 ppt) treatment. Additionally, the combined effect of pH (8.1, 7.6), salinity (24 and 34 ppt) and temperature (24 °C and 30 °C) was examined using factorial experimental design. Surprisingly, the early growth phase from hatching to 5-day-old veliger stage showed high tolerance to pH 7.9 and pH 7.6 at both 34 ppt and 27 ppt. Larval shell area was significantly smaller at pH 7.4 only in low-salinity. In the 3-factor experiment, shell area was affected by salinity and the interaction between salinity and temperature but not by other combinations. Larvae produced the largest shell at the elevated temperature in low-salinity, regardless of pH. Thus the growth of the Portuguese oyster larvae appears to be robust to near-future pH level (> 7.6) when combined with projected elevated temperature and low-salinity in the coastal aquaculture zones of South China Sea.

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.

Elevated CO2 alters larval proteome and its phosphorylation status in the commercial oyster, Crassostrea hongkongensis

Ocean acidification (OA) is beginning to have noticeable negative impact on calcification rate, shell structure and physiological energy budgeting of several marine organisms; these alter the growth of many economically important shellfish including oysters. Early life stages of oysters may be particularly vulnerable to OA-driven low pH conditions because their shell is made up of the highly soluble form of calcium carbonate (CaCO3) mineral, aragonite. Our long-term CO2 perturbation experiment showed that larval shell growth rate of the oyster species Crassostrea hongkongensis was significantly reduced at pH < 7.9 compared to the control (8.2). To gain new insights into the underlying mechanisms of low-pH-induced delays in larval growth, we have examined the effect of pH on the protein expression pattern, including protein phosphorylation status at the pediveliger larval stage. Using two-dimensional electrophoresis and mass spectrometry, we demonstrated that the larval proteome was significantly altered by the two low pH treatments (7.9 and 7.6) compared to the control pH (8.2). Generally, the number of expressed proteins and their phosphorylation level decreased with low pH. Proteins involved in larval energy metabolism and calcification appeared to be down-regulated in response to low pH, whereas cell motility and production of cytoskeletal proteins were increased. This study on larval growth coupled with proteome change is the first step toward the search for novel Protein Expression Signatures indicative of low pH, which may help in understanding the mechanisms involved in low pH tolerance.

Spider crab Hyas araneus larval dry weight, C/N ratio and developmental time during experiments from different latitudes (54° vs 79°N), 2010

The combined impacts of future scenarios of ocean acidification and global warming on the larvae of a cold-eurythermal spider crab, Hyas araneus L., were investigated in one of its southernmost populations (living around Helgoland, southern North Sea, 54°N) and one of the northernmost populations (Svalbard, North Atlantic, 79°N). Larvae were exposed at temperatures of 3, 9 and 15°C to present day normocapnia (380 ppm CO2) and to CO2 conditions expected for the near or medium-term future (710 ppm by 2100 and 3000 ppm CO2 by 2300 and beyond). Larval development time and biochemical composition were studied in the larval stages Zoea I, II, and Megalopa. Permanent differences in instar duration between both populations were detected in all stages, likely as a result of evolutionary temperature adaptation. With the exception of Zoea II at 3°C and under all CO2 conditions, development in all instars from Svalbard was delayed compared to those from Helgoland, under all conditions. Most prominently, development was much longer and fewer specimens morphosed to the first crab instar in the Megalopa from Svalbard than from Helgoland. Enhanced CO2 levels (710 and particularly 3000 ppm), caused extended duration of larval development and reduced larval growth (measured as dry mass) and fitness (decreasing C/N ratio, a proxy of the lipid content). Such effects were strongest in the zoeal stages in Svalbard larvae, and during the Megalopa instar in Helgoland larvae.

Impact of ocean acidification and warming on the larval development of the spider crab Hyas araneus from different latitudes (54° vs 79°N), 2010

The combined impacts of future scenarios of ocean acidification and global warming on the larvae of a cold-eurythermal spider crab, Hyas araneus L., were investigated in one of its southernmost populations (living around Helgoland, southern North Sea, 54°N) and one of the northernmost populations (Svalbard, North Atlantic, 79°N). Larvae were exposed at temperatures of 3, 9 and 15°C to present day normocapnia (380 ppm CO2) and to CO2 conditions expected for the near or medium-term future (710 ppm by 2100 and 3000 ppm CO2 by 2300 and beyond). Larval development time and biochemical composition were studied in the larval stages Zoea I, II, and Megalopa. Permanent differences in instar duration between both populations were detected in all stages, likely as a result of evolutionary temperature adaptation. With the exception of Zoea II at 3°C and under all CO2 conditions, development in all instars from Svalbard was delayed compared to those from Helgoland, under all conditions. Most prominently, development was much longer and fewer specimens morphosed to the first crab instar in the Megalopa from Svalbard than from Helgoland. Enhanced CO2 levels (710 and particularly 3000 ppm), caused extended duration of larval development and reduced larval growth (measured as dry mass) and fitness (decreasing C/N ratio, a proxy of the lipid content). Such effects were strongest in the zoeal stages in Svalbard larvae, and during the Megalopa instar in Helgoland larvae.

Interactive effects of ocean acidification, elevated temperature, and reduced salinity on early-life stages of the Pacific oyster

Ocean acidification (OA) effects on larvae are partially attributed for the rapidly declining oyster production in the Pacific Northwest region of the United States. This OA effect is a serious concern in SE Asia, which produces >80% of the world's oysters. Because climate-related stressors rarely act alone, we need to consider OA effects on oysters in combination with warming and reduced salinity. Here, the interactive effects of these three climate-related stressors on the larval growth of the Pacific oyster, Crassostrea gigas, were examined. Larvae were cultured in combinations of temperature (24 and 30 °C), pH (8.1 and 7.4), and salinity (15 psu and 25 psu) for 58 days to the early juvenile stage. Decreased pH (pH 7.4), elevated temperature (30 °C), and reduced salinity (15 psu) significantly delayed pre- and post-settlement growth. Elevated temperature lowered the larval lipid index, a proxy for physiological quality, and negated the negative effects of decreased pH on attachment and metamorphosis only in a salinity of 25 psu. The negative effects of multiple stressors on larval metamorphosis were not due to reduced size or depleted lipid reserves at the time of metamorphosis. Our results supported the hypothesis that the C. gigas larvae are vulnerable to the interactions of OA with reduced salinity and warming in Yellow Sea coastal waters now and in the future.

The North Sea autumn spawning Herring (Clupea harengus L.) Spawning Component Abundance Index (SCAI)

The North Sea autumn-spawning herring (Clupea harengus) stock consists of a set of different spawning components. The dynamics of the entire stock have been well characterized, but although time-series of larval abundance indices are available for the individual components, study of the dynamics at the component level has historically been hampered by missing observations and high sampling noise. A simple state-space statistical model is developed that is robust to these problems, gives a good fit to the data, and proves capable of both handling and predicting missing observations well. Furthermore, the sum of the fitted abundance indices across all components proves an excellent proxy for the biomass of the total stock, even though the model utilizes information at the individual-component level. The Orkney-Shetland component appears to have recovered faster from historic depletion events than the other components, whereas the Downs component has been the slowest. These differences give rise to changes in stock composition, which are shown to vary widely within a relatively short time. The modelling framework provides a valuable tool for studying and monitoring the dynamics of the individual components of the North Sea herring stock.

Data compilation on the biological response to ocean acidification: environmental and experimental context of data sets and related literature

The exponential growth of studies on the biological response to ocean acidification over the last few decades has generated a large amount of data. To facilitate data comparison, a data compilation hosted at the data publisher PANGAEA was initiated in 2008 and is updated on a regular basis (doi:10.1594/PANGAEA.149999). By January 2015, a total of 581 data sets (over 4 000 000 data points) from 539 papers had been archived. Here we present the developments of this data compilation five years since its first description by Nisumaa et al. (2010). Most of study sites from which data archived are still in the Northern Hemisphere and the number of archived data from studies from the Southern Hemisphere and polar oceans are still relatively low. Data from 60 studies that investigated the response of a mix of organisms or natural communities were all added after 2010, indicating a welcomed shift from the study of individual organisms to communities and ecosystems. The initial imbalance of considerably more data archived on calcification and primary production than on other processes has improved. There is also a clear tendency towards more data archived from multifactorial studies after 2010. For easier and more effective access to ocean acidification data, the ocean acidification community is strongly encouraged to contribute to the data archiving effort, and help develop standard vocabularies describing the variables and define best practices for archiving ocean acidification data.

Seawater carbonate chemistry and sea urchin Paracentrotus lividus biological processes during experiments, 2011

Ocean acidification is predicted to have significant effects on benthic calcifying invertebrates, in particular on their early developmental stages. Echinoderm larvae could be particularly vulnerable to decreased pH, with major consequences for adult populations. The objective of this study was to understand how ocean acidification would affect the initial life stages of the sea urchin Paracentrotus lividus, a common species that is widely distributed in the Mediterranean Sea and the NE Atlantic. The effects of decreased pH (elevated PCO2) were investigated through physiological and molecular analyses on both embryonic and larval stages. Eggs and larvae were reared in Mediterranean seawater at six pH levels, i.e. pHT 8.1, 7.9, 7.7, 7.5, 7.25 and 7.0. Fertilization success, survival, growth and calcification rates were monitored over a 3 day period. The expression of genes coding for key proteins involved in development and biomineralization was also monitored. Paracentrotus lividus appears to be extremely resistant to low pH, with no effect on fertilization success or larval survival. Larval growth was slowed when exposed to low pH but with no direct impact on relative larval morphology or calcification down to pHT 7.25. Consequently, at a given time, larvae exposed to low pH were present at a normal but delayed larval stage. More surprisingly, candidate genes involved in development and biomineralization were upregulated by factors of up to 26 at low pH. Our results revealed plasticity at the gene expression level that allows a normal, but delayed, development under low pH conditions.

Physiology, growth and development of larval krill ''Euphausia superba'' in autumn and winter in the Lazarev Sea, Antarctica

The physiological condition of larval Antarctic krill was investigated during austral autumn 2004 and winter 2006 in the Lazarev Sea, to provide better understanding of a critical period of their life cycle. The condition of larvae was quantified in both seasons by determining their body length (BL), dry mass (DM), elemental- and biochemical composition, as well as stomach content analysis, and rates of metabolism and growth. Overall the larvae in autumn were in better condition under the ice than in open water, and for those under the ice there was a decrease in condition from autumn to winter. Thus growth rates of furcilia larvae in open water in autumn were similar to winter values under the ice (mean 0.008 mm/d), whereas autumn, under ice values were higher: 0.015 mm/d. Equivalent larval stages had up to 30% lower BL and 70% lower DM in winter compared to autumn, with mean oxygen consumption 44% lower (0.54 µl O2 DM/h). However, their ammonium excretion rates doubled (from 0.03-0.06 µg NH4 DM/h) so their mean O:N ratio was 46 in autumn and 15 in winter. Thus differing metabolic substrates were used between autumn and winter, suggesting a flexible overwintering strategy, as suggested for adults. The larvae were eating small copepods (Oithona spp.) and/or protozoans as well as autotrophic food under the ice. However, pelagic Chlorophyll a (Chl a) was a good predictor for growth in both seasons. The physics (current speed/ice topography) probably has a critical part to play in whether larval krill can exploit the food that may be associated with sea ice or be advected away from such suitable feeding habitat.

Seawater carbonate chemistry, larval settlement and growth rate during experiments with coral Porites astreoides, 2008

In response to the increases in pCO2 projected in the 21st century, adult coral growth and calcification are expected to decrease significantly. However, no published studies have investigated the effect of elevated pCO2 on earlier life history stages of corals. Porites astreoides larvae were collected from reefs in Key Largo, Florida, USA, settled and reared in controlled saturation state seawater. Three saturation states were obtained, using 1 M HCl additions, corresponding to present (380 ppm) and projected pCO2 scenarios for the years 2065 (560 ppm) and 2100 (720 ppm). The effect of saturation state on settlement and post-settlement growth was evaluated. Saturation state had no significant effect on percent settlement; however, skeletal extension rate was positively correlated with saturation state, with ~50% and 78% reductions in growth at the mid and high pCO2 treatments compared to controls, respectively.