Marine Mussels. Elizabeth Gosling

is because the majority of studies done to date have measured single‐species responses on one stage in the life cycle, without considering the synergistic effects of other stressors (i.e. temperature, hypoxia, food concentration) and have not considered the potential for species to adapt, nor the underlying mechanisms responsible for adaptation or acclimation. In order to fully understand the consequences of ocean acidification at the population and ecosystem level, multi‐generational and multi‐stressor experiments on multiple species from geographically distinct locations are needed to assess the adaptive capacity of shelled mollusc species and the potential winners and losers in an acidifying ocean over the next century.

       (Gazeau et al. 2013, p. 2239)

The high economic value of bivalves for aquaculture has stimulated a number of studies to estimate their adaptation potential to future oceanic conditions (Parker et al. 2012, 2013, 2015; Sunday et al. 2011, 2014; Thomsen et al. 2017; Vargas et al. 2017). To illustrate, Thomsen et al. (2017) recorded the successful settlement of wild mussel larvae (M. edulis) in a periodically CO₂‐enriched habitat. The larval fitness of the population originating from the enriched habitat was compared to the response of a population from a nonenriched one. The high CO₂‐adapted population showed higher fitness under elevated pCO₂ than the nonadapted cohort, demonstrating, for the first time, an evolutionary response of a natural mussel population to OA. To assess the rate of adaptation, the authors performed a selection experiment over three generations. Tolerance to CO₂ differed substantially between the families within the F1 generation, and survival was drastically decreased in the highest – yet, realistic – pCO₂ treatment. Selection of CO₂‐tolerant F1 mussels resulted in higher calcification performance of F1 larvae during early shell formation but did not improve overall survival. Hence, the results reveal significant short‐term selective responses of traits directly affected by OA and long‐term adaptation potential in a key bivalve species. Because immediate response to selection did not directly translate into increased fitness, multigenerational studies need to take into consideration the multivariate nature of selection acting in natural habitats. Combinations of short‐term selection with long‐term adaptation in populations from CO₂‐enriched versus nonenriched natural habitats represent promising approaches toward estimating the adaptive potential of organisms facing global change.

      Hypoxia

      Another serious consequence of global warming that has gained attention only in the last two decades is the decrease in dissolved O₂ content of the world’s oceans (Keeling et al. 2010; Levin & Le Bris 2015). Global ocean deoxygenation is a direct effect of warming. A warmer ocean is more stratified because warm water is less dense than cold water, and strong density gradients reduce vertical mixing. The combined effects of reduced oxygen solubility in warmer water and increased thermal stratification create widespread oxygen reduction, termed ‘hypoxia’ or ‘deoxygenation’. In coastal and inland waters, nutrient input from wastewater treatment plants, runoff from farmland, urban and suburban areas and air pollution from cars and so forth exacerbates the problem, because nutrients can lead to the proliferation of primary production and consequently enhance reduction of dissolved oxygen (DO) by microbes (Jewett & Romanou 2017). Increased stratification leads to reduced mixing of oxygen into the ocean interior and accounts for up to 85% of global ocean oxygen loss (Helm et al. 2011). Effects of ocean temperature change and stratification on oxygen loss are strongest in intermediate or mode waters (nearly vertically homogeneous) at bathyal depths (generally 200–3000 m), and also nearshore and in the open ocean; these changes are especially evident in tropical and subtropical waters globally, in the eastern Pacific and in the Southern Ocean (Jewett & Romanou 2017).

      Hypoxic zones are areas in the ocean where the oxygen concentration is so low that animals can suffocate and die, and as a result are often called ‘dead zones’ (Diaz 2013). The largest hypoxic zone in the United States, and the second largest worldwide, occurs in the northern Gulf of Mexico adjacent to the Mississippi River. Diaz & Rosenberg (2008) assembled a global database of over 400 dead zones, a number that has not increased much since (415 in 2020). They predicted that global warming could cause dead zones to grow by a factor of 10 or more by the year 2100. Notable dead zones include the Gulf of Mexico, the Atlantic coast of North America, the east China Sea and, in European waters, the Adriatic Sea, the German Bight, the Baltic Sea and parts of the Black Sea. However, it has been demonstrated that decreased nutrient loading strongly decreases the probability of hypoxic events (Mee et al. 2005; Kemp et al. 2009). Several mitigation programmes are currently underway to reduce nutrient loading into the Gulf of Mexico, Chesapeake Bay on the Atlantic coast of the United States, and the Baltic and Black Seas.

There is growing awareness that low‐oxygen regions of the ocean are also acidified as a result of warming‐enhanced biological respiration. While the effects of hypoxia on marine mussels are well documented (see Chapter 7), the combined effects of low oxygen and acidification were until recently largely unknown. This is now an area of active research in bivalves (Meire et al. 2013; Melzner et al. 2013) and marine mussels (Gu et al. 2019; Sui et al. 2017). As seen earlier, OA can pose negative effects for the physiological energetics of mussels (Navarro et al. 2013). Therefore, it may interact with hypoxia synergistically to cause much stronger effects than those of each in isolation. To test this, Gu et al. (2019) evaluated the interactive effects of elevated CO₂ and hypoxia on physiological energetics in M. edulis. Adult mussels from the East China Sea were exposed to three pH levels (8.1, 7.7, 7.3) at two dissolved oxygen (DO) levels (6 and 2 mg L⁻¹). Clearance rate, absorption efficiency, respiration rate, excretion rate, SFG and O:N ratio were measured during a14‐day exposure time. After exposure, all parameters except excretion rate were significantly reduced under low‐pH and hypoxic conditions, while excretion rate was significantly increased. Additive effects of low pH and hypoxia were evident for all parameters, and low pH appeared to elicit a stronger effect than hypoxia (2 mg L⁻¹). Overall, the study showed that hypoxia can aggravate the effects of acidification and that its impacts on physiology and SFG may have ecological and economic ramifications in the short term.

      Sui et al. (2017) investigated the combined effects of hypoxia and OA on the defence responses of adult M. coruscus in the East China Sea, one of the largest coastal hypoxic zones observed in the world (Chen et al. 2007). Mussels were exposed to three pH/pCO₂ levels (7.3/2800 μatm, 7.7/1020 μatm and 8.1/376 μatm) at two DO concentrations (6 and 2 mg L⁻¹) for 72 hr. Results showed that byssus thread parameters (e.g. number, diameter, attachment strength, plaque area) were reduced by low DO, and shell‐closing strength was significantly weaker under both hypoxia and low‐pH conditions. Expression patterns of genes related to mussel byssus proteins were affected by hypoxia. Generally, hypoxia reduced expressions of some of these and increased expression of others. Overall, both hypoxia and low pH induced negative effects on mussel defense responses, with hypoxia being the main driver of change. In addition, significant interactive effects between pH and DO were observed on shell‐closing strength. Depressed byssus attachment strength and shell‐closing strength may enable predators and water currents to remove mussels from the substrate more easily. In a similar study, the effects of hypoxia and salinity on antipredator responses were examined in juvenile P. viridis from Hong Kong coastal waters (Wang et al. 2012). In hypoxic and low‐salinity conditions, P. viridis produced fewer byssal threads and had a thinner shell and adductor muscle, indicating that hypoxia and low salinity are severe environmental stressors for self‐defence of mussels, and that their interactive effects further increase the predation risk.

      Growing human pressures, including climate change, are having profound and diverse consequences for marine ecosystems (Doney et al. 2012). Rising atmospheric carbon dioxide is one of the most critical problems, because its effects are globally pervasive and irreversible on ecological time scales. The primary direct consequences are increasing ocean temperatures and acidity. Also, both warming and altered ocean circulation act to reduce subsurface oxygen concentrations. Furthermore, climbing temperatures