Evolved differences in energy metabolism and growth dictate the impacts of ocean acidification on abalone aquaculture

Significance

The pH of the global ocean is decreasing due to the absorption of anthropogenically emitted CO ₂, causing ocean acidification (OA). OA negatively impacts marine shellfish and threatens the continuing economic viability of molluscan shellfish aquaculture, a global industry valued at more than 19 billion USD. We identify traits linked to growth and lipid regulation that contribute tolerance to OA in abalone aquaculture, with broader implications for adaptation efforts in other shellfish species. We also identify evolved heritable variation for physiological resilience to OA that may be exploited in commercial and restoration aquaculture breeding programs to offset the negative consequences of continuing climate change.

Abstract

Ocean acidification (OA) poses a major threat to marine ecosystems and shellfish aquaculture. A promising mitigation strategy is the identification and breeding of shellfish varieties exhibiting resilience to acidification stress. We experimentally compared the effects of OA on two populations of red abalone ( Haliotis rufescens), a marine mollusc important to fisheries and global aquaculture. Results from our experiments simulating captive aquaculture conditions demonstrated that abalone sourced from a strong upwelling region were tolerant of ongoing OA, whereas a captive-raised population sourced from a region of weaker upwelling exhibited significant mortality and vulnerability to OA. This difference was linked to population-specific variation in the maternal provisioning of lipids to offspring, with a positive correlation between lipid concentrations and survival under OA. This relationship also persisted in experiments on second-generation animals, and larval lipid consumption rates varied among paternal crosses, which is consistent with the presence of genetic variation for physiological traits relevant for OA survival. Across experimental trials, growth rates differed among family lineages, and the highest mortality under OA occurred in the fastest growing crosses. Identifying traits that convey resilience to OA is critical to the continued success of abalone and other shellfish production, and these mitigation efforts should be incorporated into breeding programs for commercial and restoration aquaculture.