Does seawater acidification affect survival, growth and shell integrity in bivalve juveniles?

Anthropogenic emissions of carbon dioxide are leading to decreases in pH and changes in the carbonate chemistry of seawater. Ocean acidification may negatively affect the ability of marine organisms to produce calcareous structures while also influencing their physiological responses and growth. The aim of this study was to evaluate the effects of reduced pH on the survival, growth and shell integrity of juveniles of two marine bivalves from the Northern Adriatic sea: the Mediterranean mussel Mytilus galloprovincialis and the striped venus clam Chamelea gallina. An outdoor flow-through plant was set up and two pH levels (natural seawater pH as a control, pH 7.4 as the treatment) were tested in long-term experiments. Mortality was low throughout the first experiment for both mussels and clams, but a significant increase, which was sensibly higher in clams, was observed at the end of the experiment (6 months). Significant decreases in the live weight (-26%) and, surprisingly, in the shell length (-5%) were observed in treated clams, but not in mussels. In the controls of both species, no shell damage was ever recorded; in the treated mussels and clams, damage proceeded via different modes and to different extents. The severity of shell injuries was maximal in the mussels after just 3 months of exposure to a reduced pH, whereas it progressively increased in clams until the end of the experiment. In shells of both species, the damaged area increased throughout the experiment, peaking at 35% in mussels and 11% in clams. The shell thickness of the treated and control animals significantly decreased after 3 months in clams and after 6 months in mussels. In the second experiment (3 months), only juvenile mussels were exposed to a reduced pH. After 3 months, the mussels at a natural pH level or pH 7.4 did not differ in their survival, shell length or live weight. Conversely, shell damage was clearly visible in the treated mussels from the 1st month onward. Monitoring the chemistry of seawater carbonates always showed aragonite undersaturation at 7.4 pH, whereas calcite undersaturation occurred in only 37% of the measurements. The present study highlighted the contrasting effects of acidification in two bivalve species living in the same region, although not exactly in the same habitat.

Experiment: Marine fungi may benefit from ocean acidification

Recent studies have discussed the consequences of ocean acidification for bacterial processes and diversity. However, the decomposition of complex substrates in marine environments, a key part of the flow of energy in ecosystems, is largely mediated by marine fungi. Although marine fungi have frequently been reported to prefer low pH levels, this group has been neglected in ocean acidification research. We present the first investigation of direct pH effects on marine fungal abundance and community structure. In microcosm experiments repeated in 2 consecutive years, we incubated natural North Sea water for 4 wk at in situ seawater pH (8.10 and 8.26), pH 7.82 and pH 7.67. Fungal abundance was determined by colony forming unit (cfu) counts, and fungal community structure was investigated by the culture-independent fingerprint method Fungal Automated Ribosomal Intergenic Spacer Analysis (F-ARISA). Furthermore, pH at the study site was determined over a yearly cycle. Fungal cfu were on average 9 times higher at pH 7.82 and 34 times higher at pH 7.67 compared to in situ seawater pH, and we observed fungal community shifts predominantly at pH 7.67. Currently, surface seawater pH at Helgoland Roads remains >8.0 throughout the year; thus we cannot exclude that fungal responses may differ in regions regularly experiencing lower pH values. However, our results suggest that under realistic levels of ocean acidification, marine fungi will reach greater importance in marine biogeochemical cycles. The rise of this group of organisms will affect a variety of biotic interactions in the sea.

Ocean acidification impairs vermetid reef recruitment

Vermetids form reefs in sub-tropical and warm-temperate waters that protect coasts from erosion, regulate sediment transport and accumulation, serve as carbon sinks and provide habitat for other species. The gastropods that form these reefs brood encapsulated larvae; they are threatened by rapid environmental changes since their ability to disperse is very limited. We used transplant experiments along a natural CO2 gradient to assess ocean acidification effects on the reef-building gastropod Dendropoma petraeum. We found that although D. petraeum were able to reproduce and brood at elevated levels of CO2, recruitment success was adversely affected. Long-term exposure to acidified conditions predicted for the year 2100 and beyond caused shell dissolution and a significant increase in shell Mg content. Unless CO2 emissions are reduced and conservation measures taken, our results suggest these reefs are in danger of extinction within this century, with significant ecological and socioeconomic ramifications for coastal systems.

Seawater carbonate chemistry, fertilization and early development of the coral eating crown-of-thorns starfish, Acanthaster planci in a laboratory experiment

Outbreaks of crown-of-thorns starfish (COTS), Acanthaster planci, contribute to major declines of coral reef ecosystems throughout the Indo-Pacific. As the oceans warm and decrease in pH due to increased anthropogenic CO2 production, coral reefs are also susceptible to bleaching, disease and reduced calcification. The impacts of ocean acidification and warming may be exacerbated by COTS predation, but it is not known how this major predator will fare in a changing ocean. Because larval success is a key driver of population outbreaks, we investigated the sensitivities of larval A. planci to increased temperature (2-4 °C above ambient) and acidification (0.3-0.5 pH units below ambient) in flow-through cross-factorial experiments (3 temperature × 3 pH/pCO2 levels). There was no effect of increased temperature or acidification on fertilization or very early development. Larvae reared in the optimal temperature (28 °C) were the largest across all pH treatments. Development to advanced larva was negatively affected by the high temperature treatment (30 °C) and by both experimental pH levels (pH 7.6, 7.8). Thus, planktonic life stages of A. planci may be negatively impacted by near-future global change. Increased temperature and reduced pH had an additive negative effect on reducing larval size. The 30 °C treatment exceeded larval tolerance regardless of pH. As 30 °C sea surface temperatures may become the norm in low latitude tropical regions, poleward migration of A. planci may be expected as they follow optimal isotherms. In the absence of acclimation or adaptation, declines in low latitude populations may occur. Poleward migration will be facilitated by strong western boundary currents, with possible negative flow-on effects on high latitude coral reefs. The contrasting responses of the larvae of A. planci and those of its coral prey to ocean acidification and warming are considered in context with potential future change in tropical reef ecosystems.

Functional consequences of prey acclimation to ocean acidification for the prey and its predator

Ocean acidification is the suite of chemical changes to the carbonate system of seawater as a consequence of anthropogenic carbon dioxide (CO2) emissions. Despite a growing body of evidences demonstrating the negative effects of ocean acidification on marine species, the consequences at the ecosystem level are still unclear. One factor limiting our ability to upscale from species to ecosystem is the poor mechanistic understanding of the functional consequences of the observed effects on organisms. This is particularly true in the context of species interactions. The aim of this work was to investigate the functional consequence of the exposure of a prey (the mussel Brachidontes pharaonis) to ocean acidification for both the prey and its predator (the crab Eriphia verrucosa). Mussels exposed to pH 7.5 for >4 weeks showed significant decreases in condition index and in mechanical properties (65% decrease in maximum breaking load) as compared with mussels acclimated to pH 8.0. This translated into negative consequences for the mussel in presence of the predator crab. The crab feeding efficiency increased through a significant 27% decrease in prey handling time when offered mussels acclimated to the lowest pH. The predator was also negatively impacted by the acclimation of the prey, probably as a consequence of a decreased food quality. When fed with prey acclimated under decreased pH for 3 months, crab assimilation efficiency significantly decreased by 30% and its growth rate was 5 times slower as compared with crab fed with mussels acclimated under high pH. Our results highlight the important to consider physiological endpoints in the context of species interactions.

Larval development of the barnacle Amphibalanus improvisus responds variably but robustly to near-future ocean acidification

Increasing atmospheric CO2 decreases seawater pH in a phenomenon known as ocean acidification. In two separate experiments we found that larval development of the barnacle Amphibalanus (Balanus) improvisus was not significantly affected by the level of reduced pH that has been projected for the next 150 years. After 3 and 6 days of incubation, we found no consistent effects of reduced pH on developmental speed or larval size at pH 7.8 compared with the control pH of 8.1. After 10 days of incubation, there were no net changes in survival or overall development of larvae raised at pH 7.8 or 7.6 compared with the control pH of 8.0. In all cases, however, there was significant variation in responses between replicate batches (parental genotypes) of larvae, with some batches responding positively to reduced pH. Our results suggest that the non-calcifying larval stages of A. improvisus are generally tolerant to near-future levels of ocean acidification. This result is in line with findings for other barnacle species and suggests that barnacles do not show the greater sensitivity to ocean acidification in early life history reported for other invertebrate species. Substantial genetic variability in response to low pH may confer adaptive benefits under future ocean acidification.

Coral calcifying fluid pH dictates response to ocean acidification

Ocean acidification driven by rising levels of CO2 impairs calcification, threatening coral reef growth. Predicting how corals respond to CO2 requires a better understanding of how calcification is controlled. Here we show how spatial variations in the pH of the internal calcifying fluid (pHcf) in coral (Stylophora pistillata) colonies correlates with differential sensitivity of calcification to acidification. Coral apexes had the highest pHcf and experienced the smallest changes in pHcf in response to acidification. Lateral growth was associated with lower pHcf and greater changes with acidification. Calcification showed a pattern similar to pHcf, with lateral growth being more strongly affected by acidification than apical. Regulation of pHcf is therefore spatially variable within a coral and critical to determining the sensitivity of calcification to ocean acidification.

Elevated CO2 affects embryonic development and larval phototaxis in a temperate marine fish

As an effect of anthropogenic CO2 emissions, the chemistry of the world's oceans is changing. Understanding how this will affect marine organisms and ecosystems are critical in predicting the impacts of this ongoing ocean acidification. Work on coral reef fishes has revealed dramatic effects of elevated oceanic CO2 on sensory responses and behavior. Such effects may be widespread but have almost exclusively been tested on tropical reef fishes. Here we test the effects elevated CO2 has on the reproduction and early life history stages of a temperate coastal goby with paternal care by allowing goby pairs to reproduce naturally in an aquarium with either elevated (ca 1400 µatm) CO2 or control seawater (ca 370 µatm CO2). Elevated CO2 did not affect the occurrence of spawning nor clutch size, but increased embryonic abnormalities and egg loss. Moreover, we found that elevated CO2 significantly affected the phototactic response of newly hatched larvae. Phototaxis is a vision-related fundamental behavior of many marine fishes, but has never before been tested in the context of ocean acidification. Our findings suggest that ocean acidification affects embryonic development and sensory responses in temperate fishes, with potentially important implications for fish recruitment.

Juvenile sea stars exposed to acidification decrease feeding and growth with no acclimation potential

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.