The effect of CO2-induced ocean acidification on calcification rates and shell properties of two species of bimineralic marine calcifiers

Two-month laboratory experiments were conducted to investigate the effect of CO2-induced reductions in seawater CaCO3 saturation state on the calcification rate and skeletal properties of two bimineralic species of marine calcifiers: the serpulid tube worm Hydroides crucigera and the whelk Urosalpinx cinerea. The CaCO3 saturation states of the experimental seawaters, constrained by intercalibrated determinations of pH, alkalinity, and DIC, were attained with bubbled air-CO2 mixtures of 400 (ambient), 600, 900, and 2850 ppm pCO2, yielding Ω-aragonite of 2.5 (ambient), 2.0, 1.5, and 0.7, respectively. The organisms investigated in the present study accrete bimineralic shells of layered aragonite and calcite (whelk = low-Mg calcite; serpulid worm tube = high-Mg calcite). Buoyant weighing of the organisms at the beginning and end of the experiment revealed that their net rates of calcification decreased with increasing pCO2. A Ba-137 isotope spike added to the seawater and incorporated into the shell at the start of the experiment revealed that both species continued accreting new shell material along their zones of calcification under each of the 4 pCO2 treatments. However, linear extension rates measured relative to the Ba-137 spike declined with increasing pCO2. Powder X-ray diffraction (XRD) of the organisms’ bimineralic shells revealed increasing calcite:aragonite ratios with increasing pCO2. Synchrotron micro-XRD also revealed that the micron-scale distribution of calcite and aragonite within the shells of both organisms varied as a function of pCO2. Calcite Mg/Ca ratios, inferred from d-spacing of the calcite crystal lattice, increased with pCO2 for the high-Mg-calcite-accreting serpulid worms, yet were unaffected for the low-Mg-calcite-accreting whelks. Scanning electron microscopy (SEM) of the shells of both organisms revealed evidence of dissolution of the more soluble CaCO3 phases under the highest pCO2 treatment (2850 ppm). SEM images also revealed that CaCO3 crystal geometry and habit varied with pCO2. Biomechanical tests of the organisms’ shells revealed a decrease in both hardness and fracture resistance with increasing pCO2, which is likely attributable to partial dissolution of the more soluble phases of the organisms’ shells and/or changes in the geometry and habit of the shells’ constituent crystals. Most calcareous marine invertebrates and algae are thought to have evolved calcareous shells, tests, and skeletons to deter predation. Layered bimineralic shells, such as those produced by the whelk and serpulid worm investigated here, are thought to confer additional protection by interrupting crack-propagation and by dispersing loads throughout a more heterogeneous and complex matrix, which should effectively dissipate and/or dampen external forces. This work reveals that CO2-induced reduction in the CaCO3 saturation state of seawater not only reduces the rate at which these organisms accrete their protective shells, but also that it compromises the unique biomechanical properties of their layered bimineralic shells.