mesocosms that could provide insights into the short‐ and long‐term responses at the ecosystem level. Since their metastudy, there has been an enormous increase in the number of studies examining the effects of OA on a range of marine species, particularly the calcifying ones. The following paragraphs provide a selection of such studies, with the emphasis on those dealing with marine mussels.
To the best of my knowledge, all studies on the potential effects of OA on marine mussels are laboratory‐based. Impacts of pH on M. edulis and their larvae have been widely investigated. Thomsen & Melzner (2010) analysed the impacts of pH on metabolism in adult M. edulis. They observed reduced shell growth under severe acidification, and suggested this may be a result of synergistic effects of increased cellular energy demand and nitrogen loss. In a study on the effects of OA on early life stages of M. edulis, Gazeau et al. (2010) showed negative impacts of increasing seawater acidity on parameters such as hatching rates and D‐veliger shell growth, while Kapsenberg et al. (2018) observed abnormal soft tissue in Mytilus D‐larvae. When early life stages of M. edulis were exposed to pH 7.6, Bechmann et al. (2011) observed no significant effect on fertilisation success, development time, shell abnormality or feeding when compared to pH 8.1. In a coupled field and laboratory study, Thomsen et al. (2013) examined the annual pCO2 (p = partial pressure) variability in Kiel Fjord, Western Baltic Sea and the combined effects of elevated pCO2 and food availability on juvenile M. edulis growth and calcification. In the laboratory experiment, mussel growth and calcification were found to chiefly depend on food supply, with only minor impacts of pCO2 up to 3350 μatm. In the field growth experiment in Kiel Fjord, a brackish and CO2‐enriched habitat, the authors found seven times higher growth and calcification rates of M. edulis at a high‐CO2 inner fjord field station (mean pCO2 ~1000 μatm) in comparison to a low‐CO2 outer fjord station (~600 μatm). High mussel productivity at the inner fjord site was enabled by higher particulate organic carbon concentrations. Thomsen et al. (2013) concluded that benthic stages of M. edulis tolerate high ambient pCO2 when food supply is abundant and that energy availability needs to be considered to predict species vulnerability to OA.
In a subsequent study, Ventura et al. (2016) investigated the effects of a wide range of seawater pHs on different physiological parameters of M. edulis developing larvae in order to find the physiological tipping point beyond which they are no longer capable of carrying out the functions necessary to their survival and recruitment into the adult population. The results confirmed that decreasing seawater pH and decreasing calcium carbonate saturation state (Ω) increase larval mortality rate and the percentage of abnormally developing larvae. Virtually no larvae reared at average pH 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 (pH ≈ 7.35, 7.6, 7.85), including in undersaturated seawater with aragonite saturation state9 (Ωa) as low as 0.54 ± 0.01 (mean ± SEM), with a tipping point for normal development identified at pHT 7.765. Also, the 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. Altogether, the results for OA impacts on mussel larvae suggest an average pH of 7.16 is beyond their physiological tolerance threshold and indicate a shift in energy allocation toward growth in some individuals, thus revealing potential OA resilience.
Navarro et al. (2013) evaluated the impact of medium‐term (70 days) exposure to elevated pCO2 levels (380, 750 and 1200 ppm) on physiological processes of juvenile M. chilensis. SFG was reduced by 13% at 750 ppm and 28% at 1200 ppm CO2 compared to the control treatment, 380 ppm (see Figure 6.21). This could represent a significant loss in annual production for commercial operations. A reduction in growth to 55% was also reported for juvenile and adult M. edulis maintained under long‐term moderate CO2 levels (Michaelidis et al. 2005). Subsequently, Navarro et al. (2016) examined the combined effect of temperature (12 and 16 °C) and elevated pCO2 levels (380, 750 and 1000 μatm) on juvenile M. chilensis. They found, as in their previous study, that SFG was significantly lower at the highest pCO2 concentration compared with the control, and mussels exposed to 700 μatm did not show a significantly different SFG from the other two treatments. SFG was significantly higher at 16 °C than at 12 °C, which may be because these temperatures are within the thermal tolerance of M. chilensis in southern Chile. When strong pCO2 stress was coupled to food limitation, each significantly decreased shell length growth, and both significantly influenced the magnitude of inner shell surface dissolution in M. edulis (Melzner et al. 2011). In contrast, Range et al. (2012) found that even under extreme levels of CO2‐induced acidification, juvenile M. galloprovincialis can continue to calcify and grow.
Several studies have examined the combined effects of warming and OA on mussel growth. In one, adult mussels (M. galloprovincialis) were exposed to low and high pCO2 and 12, 14, 16, 18, 20 and 24 °C for one month (Kroeker et al. 2014). Although high pCO2 significantly reduced mussel growth at 14 °C, this effect gradually lessened with increasing temperature, illustrating how warming can moderate the effects of OA in this species. Similar results have also been reported for adult M. galloprovincialis (Gazeau et al. 2014) and juveniles of M. edulis (Hiebenthal et al. 2013) and M. coruscus (Wang et al. 2015). However, Vihtakari et al. (2013) found that increasing temperature might have a larger impact on sperm motility and very early larval stages in M. galloprovincialis than OA at the levels predicted for the end of the century.
In mussels, elevated pCO2 impacts on larval and broodstock feeding (Diaz et al. 2018), byssal attachment (O’Donnell et al. 2013), sea star and gastropod predation (Kepell et al. 2015; Sadler et al. 2018), anti‐predator defense strategies (Kong et al. 2019), levels of predation vulnerability (Kroeker et al. 2016), cellular signaling pathways involved in the immune response (Bibby et al. 2008), immune parameters of haemocytes (Wu et al. 2018), host–pathogen interactions (Asplund et al. 2014), antimicrobial activity (Hernroth et al. 2016) and expression of genes involved in energy and protein metabolism (Hüning et al. 2013).
As already mentioned, OA is altering the oceanic carbonate saturation state and threatening the survival of marine calcifying organisms. Production of their calcium carbonate exoskeletons is dependent not only on the environmental seawater carbonate chemistry but also on the ability to produce biominerals through proteins. A detailed description of the production and structure of mussel shells is given in Chapter 2. Fitzer et al. (2014) examined the responses of M. edulis to four pCO2 concentrations (380, 550, 750 and 1000 μatm pCO2) over a six‐month incubation period. These concentrations represent future OA scenarios leading up to the year 2100. Mussels were also exposed to combined increases in CO2 and temperature (ambient + 2 °C) relating to future projected climate change. They were examined for shell structural and crystallographic orientation, growth, calcite and aragonite (crystalline forms of calcium carbonate) thickness and carbonic anhydrase concentration. The aim of the investigation was to determine the presence of any OA ‘tipping’ point or threshold which, once reached, might cause calcifiers to experience difficulties in maintaining control of biomineralisation and producing structurally sound shell growth. In a related study, Fitzer et al. (2015) found that OA resulted in rounder, flatter mussel shells with thinner aragonite layers likely to be more vulnerable to fracture under changing environments and predation. These changes in shape could present a compensatory mechanism to enhance protection against predators and changing environments. Mussels employ transient phases of amorphous calcium carbonate (ACC) in the construction of crystalline shells. Fitzer et al. (2016) investigated the influence of OA on
