Within- and transgenerational stress legacy effects of ocean acidification on red abalone (Haliotis rufescens) growth and survival.

Understanding the mechanisms by which individual organisms respond and populations adapt to global climate change is a critical challenge. The role of plasticity and acclimation, within and across generations, may be essential given the pace of change. We investigated plasticity across generations and life stages in response to ocean acidification (OA), which poses a growing threat to both wild populations and the sustainable aquaculture of shellfish. Most studies of OA on shellfish focus on acute effects, and less is known regarding the longer term carryover effects that may manifest within or across generations. We assessed these longer term effects in red abalone (Haliotis rufescens) using a multi-generational split-brood experiment. We spawned adults raised in ambient conditions to create offspring that we then exposed to high pCO2 (1180 µatm; simulating OA) or low pCO2 (450 µatm; control or ambient conditions) during the first 3 months of life. We then allowed these animals to reach maturity in ambient common garden conditions for 4 years before returning the adults into high or low pCO2 treatments for 11 months and measuring growth and reproductive potential. Early-life exposure to OA in the F1 generation decreased adult growth rate even after 5 years especially when abalone were re-exposed to OA as adults. Adult but not early-life exposure to OA negatively impacted fecundity. We then exposed the F2 offspring to high or low pCO2 treatments for the first 3 months of life in a fully factorial, split-brood design. We found negative transgenerational effects of parental OA exposure on survival and growth of F2 offspring, in addition to significant direct effects of OA on F2 survival. These results show that the negative impacts of OA can last within and across generations, but that buffering against OA conditions at critical life-history windows can mitigate these effects.

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

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.

Plastic responses of bryozoans to ocean acidification.

Phenotypic plasticity has the potential to allow organisms to respond rapidly to global environmental change, but the range and effectiveness of these responses are poorly understood across taxa and growth strategies. Colonial organisms might be particularly resilient to environmental stressors, as organizational modularity and successive asexual generations can allow for distinctively flexible responses in the aggregate form. We performed laboratory experiments to examine the effects of increasing dissolved carbon dioxide (CO2) (i.e. ocean acidification) on the colonial bryozoan Celleporella cornuta sampled from two source populations within a coastal upwelling region of the northern California coast. Bryozoan colonies were remarkably plastic under these CO2 treatments. Colonies raised under high CO2 grew more quickly, investing less in reproduction and producing lighter skeletons when compared with genetically identical clones raised under current surface atmosphere CO2 values. Bryozoans held under high CO2 conditions also changed the Mg/Ca ratio of skeletal calcite and increased the expression of organic coverings in new growth, which may serve as protection against acidified water. We also observed strong differences between source populations in reproductive investment and organic covering reaction norms, consistent with adaptive responses to persistent spatial variation in local oceanographic conditions. Our results demonstrate that phenotypic plasticity and energetic trade-offs can mediate biological responses to global environmental change, and highlight the broad range of strategies available to colonial organisms.

Interactive effects of temperature, food and skeletal mineralogy mediate biological responses to ocean acidification in a widely distributed bryozoan.

Marine invertebrates with skeletons made of high-magnesium calcite may be especially susceptible to ocean acidification (OA) due to the elevated solubility of this form of calcium carbonate. However, skeletal composition can vary plastically within some species, and it is largely unknown how concurrent changes in multiple oceanographic parameters will interact to affect skeletal mineralogy, growth and vulnerability to future OA. We explored these interactive effects by culturing genetic clones of the bryozoan Jellyella tuberculata (formerly Membranipora tuberculata) under factorial combinations of dissolved carbon dioxide (CO2), temperature and food concentrations. High CO2 and cold temperature induced degeneration of zooids in colonies. However, colonies still maintained high growth efficiencies under these adverse conditions, indicating a compensatory trade-off whereby colonies degenerate more zooids under stress, redirecting energy to the growth and maintenance of new zooids. Low-food concentration and elevated temperatures also had interactive effects on skeletal mineralogy, resulting in skeletal calcite with higher concentrations of magnesium, which readily dissolved under high CO2 For taxa that weakly regulate skeletal magnesium concentration, skeletal dissolution may be a more widespread phenomenon than is currently documented and is a growing concern as oceans continue to warm and acidify.