This AOP is licensed under a Creative Commons Attribution 4.0 International License.
Reduced environmental pH leading to thinner shells in Mytilus edulis
- James Ducker
|Author status||OECD status||OECD project||SAAOP status|
|Under development: Not open for comment. Do not cite|
This AOP was last modified on March 17, 2020 01:15
Despite contemporary scientific efforts focusing on better understanding the consequences of ocean acidification, the overwhelming abundance of novel findings may be undermining the applications of studies. Climate research may benefit from the development of a conceptual framework synthesizing the sequential cascade of responses initiated by environmental stressors, termed Adverse Outcome Pathways (AOP) (Ankley et al., 2010).
Preliminary AOP for Mytilus edulis indicates that OA has a myriad of repercussions across biological levels, with multiple potential adverse outcomes to consider. The impacts are interconnected and demonstrate how molecular processes may affect whole-organism processes. The studies considering M. edulis provide a comprehensive AOP as it is a well-studied species, with most impacts at individual (whole-organism) level.
Based on the evidence gathered to design this AOP, the following pathway was developed from the MIE of reduced environmental pH leading to alterations in genes encoding calcification and metabolic pathways. Following such alterations, signifcant changes were documented at cellular and organ level, including an imbalance in acid-base status, which led to the deregulation of growth and development at the individual level. Ultimately, such impacts resulted in the decline of populations. However, it is essential to note that these outcomes were not observed unilaterally.
Indeed, frequent variation in outcomes was observed across studies. In particular, variations in the pathway was documented between sexes, life stages and temporal scales. Despite such variation the application of the AOP framework offers a unique perspective synthesizing our current understanding. Moreover, future research progressing our understanding on synergistic effects would further improve the efficacy of AOPs in climate research (Falkenberg et al., 2013).
Over the past two decades, it is estimated that over half of global carbon dioxide emissions has been absorbed by the oceans (Sabine et al., 2004), resulting in the average oceanic pH declining by 0.1 units compared to pre-industrial levels in a process termed ocean acidification (OA) (Caldeira et al., 2005).
Predictions have mainly focused on surface ocean waters resulting in weak representation for coastal ecosystems and taxonomic groups within them (Fabri et al., 2008) despite their socioeconomic value (Falkenberg and Tubb 2017). One such group are the molluscs, which are used as valuable ecological models and represent a taxon of widespread aqua cultural importance in coastal systems (Costanza et al., 1997). Additionally, molluscs are comparatively well studied in terms of climate related impacts and therefore provide extensive information useful to be used in novel frameworks (e.g. see review by Gazeau et al 2013).
Ocean acidification is recognised to impact the physiology, behaviour and evolution of molluscs (Kroeker et al. 2010; Gazeau et al. 2013). Organisms with calcium carbonate-based shells may be particularly susceptible due to the dependence of shell formation on pH and carbon chemistry (Beniash et al. 2010; Tomanek et al. 2011; Parker et al. 2012). However, the severity of impacts is unclear as calcifying organisms may be resilient to highly variable coastal environments (Duarte et al. 2013) and are also known to exhibit varying sensitivities depending on biological context including factors such as life stage, community composition and nutritional status (Kroeker et al., 2013). Moreover, the effects of acidification are known to synergistically interact with other anthropogenic stressors, such as toxicants (Cao et al., 2018, 2019) and climatic stressors, particularly ocean warming (Kroeker et al., 2013).
Climate research may benefit from the development of a conceptual framework synthesizing the sequential cascade of responses initiated by environmental stressors, termed Adverse Outcome Pathways (AOP) (Ankley et al., 2010). AOPs were first developed in 1992 and have been used primarily for toxicology purposes in order to collect key information on the sequential consequences of toxicants across biological processes (see Figure 1). Since being implemented, the adoption of AOPs has gained momentum leading to the design of online databases gathering information on a myriad of stressors and their impacts around the globe (https://aopwiki.org/). AOPs are used to synthesize information for actions plans, establishing risk assessments supported by empirical data on biological context and spatiotemporal trends aiming to improve risk characterization of targeted species to particular stressors (Ankley et al., 2010). To date, the AOP framework has yet to be used to address ocean acidification, with few examples applied to climate science even if AOPs can incorporate vital biological pathways impacted by climatic stressors (Hooper et al., 2013). Indeed, the effects of anthropogenic climate change (e.g. increased temperatures, hypoxia or acidification) are akin to human derived toxicants as they represent a potentially lethal threat to organisms that have yet to experience such severe and frequent alterations in environmental conditions. Thus, AOPs would provide a unique and comprehensive tool using a risk assessment approach to climate related impacts on ecosystems and the species within them (Falkenberg et al., 2018; Hooper et al., 2013).
Summary of the AOP
Molecular Initiating Events (MIE)
Key Events (KE)
Adverse Outcomes (AO)
Relationships Between Two Key Events (Including MIEs and AOs)
Life Stage Applicability
Overall Assessment of the AOP
Domain of Applicability
Acidification is recognised to impact Mytilus edulis across life stages from larval form through to adult stages. However, sensitivity varies considerably in response to acidification. In particular, embryonic and larval stages are known to be most susceptible to acidifcation, with considerable reductions in size and development resulting in higher mortality (Gazeau et al., 2013; Thomsen et al., 2015).
For the majority of bivalve species and some gastropods that are more primitive, fertilization occurs in the surrounding water; for example, eggs and sperm of bivalves are shed into the suprabranchial cavity where they are released into the water column with the exhalant current (Barnes 1974).
Our knowledge of the impacts of ocean acidification on the fertilization on broadcast spawning shelled molluscs is based on a limited number of studies (9), covering only seven species (Table 2). CO2-induced hypercapnia is believed to have a narcotic effect on sperm, reducing its speed and motility, thereby reducing fertilization success (Havenhand et al. 2008; Byrne 2011; Reuter et al. 2011).
Thus, the present AOP provides an insight into a mechanistic process capable of affecting mussels across life stages. Nonetheless, the variations described above is indicative of the consideration required to extract the exact consequences expected from acidifcation.
The effects of ocean acidification on the growth and shell production by juvenile and adult shelled molluscs are variable among species and even within the same species, precluding the drawing of a general picture (see Gazeau et al., 2013). This is, however, not the case for pteropods, with all species tested so far, being negatively impacted by ocean acidification.
Ubiquitous elements? Cellular changes, genes and reactions in other bivalves – similar? Spatiotemporal differences in populations?
The present AOP may be applicable to other bivalve species as the process of calcification is similar across taxa (REFs).
Physiology and behavioural changes for other taxa or groups
In the mussel M. edulis, for example, exposure to elevated CO2 of 1,120 latm (-0.3 pH unit) for 60 days led to a significant increase in SMR (Thomsen and Melzner 2010). In juveniles of the oyster C. virginica, exposure to elevated CO2 of *3,300 latm (-0.7 pH unit) for 20 weeks, a level much higher than that used in the previous study (and therefore not shown in Fig. 4), caused an increase in SMR which was accompanied by a decrease in both shell and somatic growth and survival (Beniash et al. 2010). A number of other shelled mollusc species have also suffered reduced survival following chronic exposure to elevated CO2 (snail S. lubuanus, Shirayama and Thornton 2005; mussel M. edulis, Berge et al. 2006; clam M. mercenaria, Green et al. 2009; oyster C. virginica, Dickinson et al. 2012; clam T. squamosa, Watson et al. 2012b).
In the limpet Patella vulgata (Marchant et al. 2010), mussels Perna viridis (Liu and He 2012) and M. galloprovincialis (Fernandez-Reiriz et al. 2012) and oyster Pinctada fucata (Liu and He 2012), there was no observable change in SMR during exposure to elevated CO2 (see Fig. 4). Trade-offs in energy allocation may still exist, however, such that metabolic stimulation occurs in one tissue whereas metabolic depression occurs in another (Lannig et al. 2010).
The data suggest for several shelled molluscan species that ocean acidification combined with ocean warming may have even greater impacts than those documented for ocean acidification alone. This is the case, for instance, for the fluted giant clam (Tridacna squamosa) which showed much lower survival when low pH was combined with higher temperature (Watson et al. 2012b).
Essentiality of the Key Events
- Biological plausibility: Is there a mechanistic (i.e. structural or functional) relationship between KEup and KE down consistent with established biological knowledge?
YES – known physiological processes
- Empirical support: Does the empirical evidence support that a change in the KEup leads to an appropriate change in the KE down? Does KEup occur at lower doses and earlier time points than KE down and is the incidence of KEup higher than that for KE down?
Type of studies?
Variation in results?
Maybe a non linear relationship between OA amount and thinning of shells
- Uncertainties and Inconsistencies: conditions for KE to be fulfilled or not, what might interfere with outcomes e.g. dose responses, individual variations, adaptation & acclimation potential
Spatiotemporal variations – biological context etc.
Increased abundance of studies in recent years.
Ample reviews on the topic considering numerous perspectives.
Finally, even identical species have shown differing responses of fertilization to ocean acidification. For example, gametes of the Pacific oyster, C. gigas, from populations in Japan (Kurihara et al. 2007) and Sweden (Havenhand and Schlegel 2009) experienced no reduction in percentage fertilization, sperm swimming speed and motility (sperm tested only in the Swedish population) when reared at elevated pCO2 of 1,000–2,300 latm (-0.3 to -0.8 pH unit).
This suggests that intraspecific variation may exist between populations due to both environmental and genetic differences that may lead to within-species differences in fertilization response to ocean acidification stress
The results of the studies to date suggest that for a number of shelled mollusc species, ocean acidification will cause a rise in the cost of maintenance and a shift in energy budgets, unless acclimation across life-history stages or evolutionary adaptation occurs. The tissue and mechanisms responsible for such cost increments have not been identified; however, comparative findings in fish gills indicate that elevated costs of ion and acid–base regulation in gill tissue may be involved (Deigweiher et al. 2009). Future studies would benefit from assessment of the effects of ocean acidification on the entire energy budget of shelled molluscs to identify whether altered partitioning of the energy budget is occurring and which critical fitness-sustaining processes will be most vulnerable.
Very few studies focusing on the effect of ocean acidification on shelled molluscs actually report on the level and on the variations in pH in the ecosystem the organisms were taken from (e.g. Thomsen et al. 2010).
Considerations for Potential Applications of the AOP (optional)
Despite being crucial physiological traits for ecological success, very little is known of the effects of ocean acidification on shelled mollusc health and the potential for shelled mollusc species to resist predators and/or disease. Bibby et al. (2008) showed an effect of acidification (-0.2 to -1.1 pH unit) on the immune response of the blue mussel (M. edulis).
Finally, differences in the accumulation of metals have also been documented in juveniles of the clam, Ruditapes philippinarum, where metal accumulation (Zn, Pb, Cu, Ni, Cr, Hg, As; but not Cd) was found to increase upon exposure to elevated pCO2 for 28 days (-1.0 pH unit; Lopez et al. 2010). This highlights the potential ecotoxicological consequences that may be associated with ocean acidification stress in addition to the developmental and physiological effects that have been documented.
In addition, shelled molluscs have a significant economic value as the global shellfish aquaculture industry reached a global value of US$ 13.1 billion in 2008 (FAO 2008). In recent decades, severe declines in shelled mollusc populations have been reported. Surveys conducted annually along the coast of British Columbia have shown a decline of up to 80 % in some populations since 1978 (Hankewich and Lessard 2006). Moreover, in hatcheries located on the northwest coast of the USA, there has been a year-by-year decline in the survival of oyster larvae since 2005, which appears to be connected to the upwelling of acidified deep waters shifting coastward and associated near-shore ocean acidification (Barton et al. 2012). Indeed, Feely et al. (2008) have noticed that even though seasonal upwelling of waters undersaturated with aragonite (one of the most soluble metastable forms of calcium carbonate) is a natural feature on the northern California shelf, the uptake of anthropogenic CO2 has increased the affected area over recent decades.