Читать книгу Marine Mussels - Elizabeth Gosling - Страница 54

Human activities such as the burning of oil, coal and gas, as well as deforestation, are the primary cause of the increased CO₂ concentrations in the atmosphere. The global average atmospheric CO₂ in 2018 was 407.4 ppm, with a range of uncertainty of ±0.1 ppm. Carbon dioxide levels today are higher than at any point in at least the past 800 000 years (NOAA Global Climate Report 2019). Human‐induced rise in atmospheric CO₂ concentration has been linked to changes in seawater carbonate chemistry and a decrease in ocean pH, a process known as ocean acidification (OA) (Ventura et al. 2016; see Chapter 6). When carbon dioxide diffuses into the ocean, it reacts with water to create carbonic acid (H₂CO₃), most of which quickly dissociates into a hydrogen ion (H⁺) and bicarbonate (HCO₃ ⁻), which can further dissociate into carbonate (CO₃ ²⁻) and hydrogen ions (Figure 3.18). Some of the carbonate ions already in the ocean combine with some of the hydrogen ions to form further bicarbonate, thereby reducing the availability of carbonate ions, which are necessary for marine calcifying organisms such as corals, foraminiferans, echinoderms, crustaceans and molluscs to produce their CaCO₃ shells and skeletons (Fabry et al. 2008).

Since the Industrial Revolution, a time span of less than 250 years, the pH of surface oceans has dropped by 0.1 pH units, representing a ~30% increase in hydrogen ion concentration relative to the preindustrial value (Guinotte & Fabry 2008). The pH scale is logarithmic, and consequently each whole unit decrease in pH is equal to a 10‐fold increase in acidity. The pH of the oceans is projected to drop another 0.3–0.4 pH units by 2100 (Mackenzie et al. 2014). The rate of this change is cause for concern, as many marine organisms – particularly those that calcify (see earlier) – may not be able to adapt quickly enough to survive. The degree of change will depend on whether we adopt a concerted rapid CO₂ mitigation effort or a ‘business‐as‐usual’ attitude (Mora et al.2013). The lowest surface ocean pH is found in the equatorial regions from 20 °N to 20 °S, especially in the eastern Pacific (Jiang et al. 2019). The Arctic Ocean shows the largest spatial variability, followed by the Southern Ocean, which surrounds Antarctica. The globally and annually averaged surface ocean pHs in the Atlantic, Pacific and Indian Oceans (60 °N to 60 °S) are very similar at 8.07 ± 0.02, 8.06 ± 0.03 and 8.07 ± 0.02, respectively, with a global average of 8.07 ± 0.02 between 60 °N to 60 °S. The most rapid acidification is presently occurring in the Arctic Ocean (see Qi et al. 2017).

Figure 3.18 Schematic diagram of ocean acidification (OA). The reaction between dissolved carbon dioxide (CO₂) and water results in an increase in the concentration of hydrogen ions (H⁺); additional changes include an increase in bicarbonate ions (HCO3–) and a great decrease in carbonate ions (CO₃²⁻). These ions will modify the carbonate saturation state, leading to acidification.

Source: From Birchenough et al. (2017). Open Government Licence v3.0.

Dupont & Pörtner (2013) reviewed a selection of papers covering a range of experimental approaches used to investigate the impact of OA on marine species and ecosystems. They found that while the vast majority of studies (>90%) on the potential effects of OA were laboratory‐based, there were a few field studies using natural gradients or CO₂‐rich environments and large‐scale field studies using 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 pH_T 7.765. Also, the growth rate of normally developing larvae was not affected by lower pH_T 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 ACC formation in the shells of adult M. edulis. Their results demonstrated that OA induces more ACC formation and less crystallographic control in mussels, suggesting that ACC is used as a repair mechanism to combat shell damage under OA. However, the resultant reduced crystallographic control in mussels raises concerns for shell protective function under predation and changing environments.

Gaylord et al. (2011) tested effects of OA on the larval stage of M. californianus, a critical community member on rocky shores of the northeastern Pacific. Larvae were cultured for eight days in seawater containing CO₂ concentrations associated with a present‐day global‐mean atmospheric concentration (~380 ppm) contrasted against a ‘fossil fuel‐intensive’ projection (970 ppm) and a more optimistic prediction (540 ppm). The authors analysed the strength, size and thickness of larval shells and found that acidification of the seawater had a strong impact on shell strength. The shells of five‐day‐old larvae raised in 970 ppm CO₂ were 20% weaker than those of larvae reared at the current CO₂ level, while the shells of larvae reared at 540 ppm CO₂ were only 13% weaker than those of control individuals. They also found that after eight days at 970 ppm CO₂, the shells were up to 15% thinner and 5% smaller, and the body mass of the mussels within the shells were as much as 33% smaller than those of mussels grown at modern levels. Potential ecological consequences of OA are larvae weakened by rising CO₂ levels, slow development, vulnerability to predation, susceptibility to stress and risk of desiccation, ultimately altering mussel survivorship and thereby overall community dynamics.

The following is a succinct summary of the current OA scenario:

Over the next decades, it is likely that ocean acidification will pose serious consequences for many marine and estuarine shelled molluscs. A comparison of the available literature to date suggests that while detrimental effects on adults remain uncertain, the most sensitive life‐history stage seems to be the larvae, with a large majority of studies on this critical stage of development revealing negative effects. Despite these obvious trends, our current understanding of the biological consequences of an acidifying ocean over the next century is still dominated by large uncertainties. This 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.