Reduced environmental pH leading to thinner shells in Mytilus edulis

Submitted by James Ducker, PhD student in Marine Biology at the Chinese University of Hong Kong (CUHK), Hong Kong SAR. 

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). 

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.

Risk assessments

Ecosystem mangament 

Conservation

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.