Mussels repair shell damage despite limitations imposed by ocean acidification

Bivalves frequently withstand shell boring attempts by predatory gastropods that result in shell damage that must be quickly repaired to ensure survival. While the processes that underlie larval shell development have been extensively studied within the context of ocean acidification (OA), it remains unclear whether shell repair is impaired by elevated pCO2. To better understand the stereotypical shell repair process, we monitored mussels (Mytilus edulis) with sublethal shell damage within both field and laboratory conditions to characterize the deposition rate, mineral composition, and structural integrity of repaired shell. These results were then compared with a laboratory experiment wherein mussels (Mytilus trossulus) repaired shell damage in one of seven pCO2 treatments (400–2500 µatm). Shell repair proceeded through four distinct stages; shell damage was first covered with an organic film, then mineralized over the course of weeks, acquiring the appearance of nacre after 8 weeks. OA did not impact the ability of mussels to close drill holes, nor the strength or density of the repaired shell after 10-weeks, as measured through mechanical testing and µCT analysis. However, as mussels progressed through each repair stage, significant interactions between pCO2, the length of exposure to treatment conditions, and the strength, inorganic content, and physiological condition of mussels within OA treatments were observed. These results suggest that, while OA may not prevent mussels from repairing shell damage, sustained exposure to elevated pCO2 may induce physiological stress responses that impose energetic constraints on the shell repair process.

Thermal plasticity of growth and chain formation of the dinoflagellates Alexandrium affine and Alexandrium pacificum with respect to ocean acidification

The amount of CO2 absorbed by the oceans continues to rise, resulting in further acidification, altering some functional traits of phytoplankton. To understand the effect of elevated partial pressures of CO2 (pCO2) on functional traits of dinoflagellates Alexandrium affine and A. pacificum, the cardinal temperatures and chain formation extent were examined under two pCO2 (400 and 1,000 μatm) over the range of temperature expected to be associated with growth. The growth rate and chain formation extent of A. affine increased with higher pCO2, showing significant changes in cardinal temperatures and a substantial increase in middle chain-length (4‒8 cells) fractionation under elevated pCO2 condition. By contrast, there were no significant differences in specific growth rate and any chain-length fractionation of A. pacificum between ambient and elevated pCO2 conditions. The observed interspecies variation in the functional traits may reflect differences in ability of species to respond to environmental change with plasticity. Moreover, it allows us to understand the shifting biogeography of marine phytoplankton and predict their phenology in the Korea Strait.

Tolerant Larvae and Sensitive Juveniles: Integrating Metabolomics and Whole-Organism Responses to Define Life-Stage Specific Sensitivity to Ocean Acidification in the American Lobster

Bentho-pelagic life cycles are the dominant reproductive strategy in marine invertebrates, providing great dispersal ability, access to different resources, and the opportunity to settle in suitable habitats upon the trigger of environmental cues at key developmental moments. However, free-dispersing larvae can be highly sensitive to environmental changes. Among these, the magnitude and the occurrence of elevated carbon dioxide (CO2) concentrations in oceanic habitats is predicted to exacerbate over the next decades, particularly in coastal areas, reaching levels beyond those historically experienced by most marine organisms. Here, we aimed to determine the sensitivity to elevated pCO2 of successive life stages of a marine invertebrate species with a bentho-pelagic life cycle, exposed continuously during its early ontogeny, whilst providing in-depth insights on their metabolic responses. We selected, as an ideal study species, the American lobster Homarus americanus, and investigated life history traits, whole-organism physiology, and metabolomic fingerprints from larval stage I to juvenile stage V exposed to different pCO2 levels. Current and future ocean acidification scenarios were tested, as well as extreme high pCO2/low pH conditions that are predicted to occur in coastal benthic habitats and with leakages from underwater carbon capture storage (CCS) sites. Larvae demonstrated greater tolerance to elevated pCO2, showing no significant changes in survival, developmental time, morphology, and mineralisation, although they underwent intense metabolomic reprogramming. Conversely, juveniles showed the inverse pattern, with a reduction in survival and an increase in development time at the highest pCO2 levels tested, with no indication of metabolomic reprogramming. Metabolomic sensitivity to elevated pCO2 increased until metamorphosis (between larval and juvenile stages) and decreased afterward, suggesting this transition as a metabolic keystone for marine invertebrates with complex life cycles.

Repeat exposure to hypercapnic seawater modifies growth and oxidative status in a tolerant burrowing clam

Whereas low levels of thermal stress, irradiance, and dietary restriction can have beneficial effects for many taxa, stress acclimation remains understudied in marine invertebrates, despite being threatened by climate change stressors such as ocean acidification. To test for life-stage and stress-intensity dependence in eliciting enhanced tolerance under subsequent stress encounters, we initially conditioned pediveliger Pacific geoduck (Panopea generosa) larvae to (i) ambient and moderately elevated pCO2 (920 µatm and 2800 µatm, respectively) for 110 days, (ii) secondarily applied a 7-day exposure to ambient, moderate, and severely elevated pCO2 (750 µatm, 2800 µatm, and 4900 µatm, respectively), followed by 7 days in ambient conditions, and (iii) implemented a 7-day third exposure to ambient (970 µatm) and moderate pCO2 (3000 µatm). Initial conditioning to moderate pCO2 stress followed by second and third exposure to severe and moderate pCO2 stress increased respiration rate, organic biomass, and shell size suggesting a stress-intensity-dependent effect on energetics. Additionally, stress-acclimated clams had lower antioxidant capacity compared to clams under ambient conditions, supporting the hypothesis that stress over postlarval-to-juvenile development affects oxidative status later in life. Time series and stress intensity-specific approaches can reveal life-stages and magnitudes of exposure, respectively, that may elicit beneficial phenotypic variation.

Adult exposure to ocean acidification and warming remains beneficial for oyster larvae following starvation

Climate change is expected to warm and acidify oceans and alter the phenology of phytoplankton, creating a mismatch between larvae and their food. Transgenerational plasticity (TGP) may allow marine species to acclimate to climate change; however, it is expected that this may come with elevated energetic demands. This study used the oysters, Saccostrea glomerata and Crassostrea gigas, to test the effects of adult parental exposure to elevated pCO2 and temperature on larvae during starvation and recovery. It was anticipated that beneficial effects of TGP will be limited when larvae oyster are starved. Transgenerational responses and lipid reserves of larvae were measured for 2 weeks. Larvae of C. gigas and S. glomerata from parents exposed to elevated pCO2 had greater survival when exposed to elevated CO2, but this differed between species and temperature. For S. glomerata, survival of larvae was greatest when the conditions experienced by larvae matched the condition of their parents. For C. gigas, survival of larvae was greater when parents and larvae were exposed to elevated pCO2. Larvae of both species used lipids when starved. The total lipid content was dependent on parental exposure and temperature. Against expectations, the beneficial TGP responses of larvae remained, despite starvation.

Diurnally fluctuating pCO2 enhances growth of a coastal strain of Emiliania huxleyi under future-projected ocean acidification conditions

The carbonate chemistry in coastal waters is more variable compared with that of open oceans, both in magnitude and time scale of its fluctuations. However, knowledge of the responses of coastal phytoplankton to dynamic changes in pH/pCO2 has been scarcely documented. Hence, we investigated the physiological performance of a coastal isolate of the coccolithophore Emiliania huxleyi (PML B92/11) under fluctuating and stable pCO2 regimes (steady ambient pCO2, 400 μatm; steady elevated pCO2, 1200 μatm; diurnally fluctuating elevated pCO2, 600–1800 μatm). Elevated pCO2 inhibited the calcification rate in both the steady and fluctuating regimes. However, higher specific growth rates and lower ratios of calcification to photosynthesis were detected in the cells grown under diurnally fluctuating elevated pCO2 conditions. The fluctuating pCO2 regime alleviated the negative effects of elevated pCO2 on effective photochemical quantum yield and relative photosynthetic electron transport rate compared with the steady elevated pCO2 treatment. Our results suggest that growth of E. huxleyi could benefit from diel fluctuations of pH/pCO2 under future-projected ocean acidification, but its calcification was reduced by the fluctuation and the increased concentration of CO2, reflecting a necessity to consider the influences of dynamic pH fluctuations on coastal carbon cycles associated with ocean global changes.

Divergent Proteomic Responses Offer Insights Into Resistant Physiological Responses of a Reef-Foraminifera to Climate Change Scenarios

Reef-dwelling calcifiers face numerous environmental stresses associated with anthropogenic carbon dioxide emissions, including ocean acidification and warming. Photosymbiont-bearing calcifiers, such as large benthic foraminifera, are particularly sensitive. To gain insight into their resistance and adaptive mechanisms to climate change, Amphistegina lobifera from the Gulf of Aqaba were cultured under elevated pCO2 (492, 963, and 3182 ppm) fully-crossed with elevated temperature (28°C and 31°C) for two months. Differential protein abundances in host and photosymbionts amongst treatments were investigated alongside physiological responses and microenvironmental pH variations. Over 1000 proteins were identified, of which one-third varied significantly between treatments. Thermal stress induced protein depletions, along with reduced holobiont growth. Elevated pCO2 caused only minor proteomic alterations and color changes. However, combined stressors reduced pore sizes and increased microenvironmental pH, indicating adaptive modifications to gas exchange. Notably, substantial proteomic variations at moderate-pCO2 and 31°C indicate cellular stress, while stable physiological performance at high-pCO2 and 31°C is scrutinized by putative decreases in test stability. Our experiment shows that the effects of climate change can be missed when stressors are assessed in isolation, and that physiological responses should be assessed across organismal levels to make more realistic predictions for the fate of reef calcifiers.