As a consequence of anthropogenic CO2-driven ocean acidification (OA), coastal waters are becoming increasingly challenging for calcifiers due to reductions in saturation states of calcium carbonate (CaCO3) minerals. The response of calcification rate is one of the most frequently investigated symptoms of OA. However, OA may also result in poor quality calcareous products through impaired calcification processes despite there being no observed change in calcification rate. The mineralogy and ultrastructure of the calcareous products under OA conditions may be altered, resulting in changes to the mechanical properties of calcified structures. Here, the warm water biofouling tubeworm, Hydroides elegans, was reared from larva to early juvenile stage at the aragonite saturation state (ΩA) for the current pCO2 level (ambient) and those predicted for the years 2050, 2100 and 2300. Composition, ultrastructure and mechanical strength of the calcareous tubes produced by those early juvenile tubeworms were examined using X-ray diffraction (XRD), Fourier transform infrared spectroscopy (FT-IR), scanning electron microscopy (SEM) and nanoindentation. Juvenile tubes were composed primarily of the highly soluble CaCO3 mineral form, aragonite. Tubes produced in seawater with aragonite saturation states near or below one had significantly higher proportions of the crystalline precursor, amorphous calcium carbonate (ACC) and the calcite/aragonite ratio dramatically increased. These alterations in tube mineralogy resulted in a holistic deterioration of the tube hardness and elasticity. Thus, in conditions where ΩA is near or below one, the aragonite-producing juvenile tubeworms may no longer be able to maintain the integrity of their calcification products, and may result in reduced survivorship due to the weakened tube protection.
Using CO2 perturbation experiments, we examined the pre- and post-settlement growth responses of a dominant biofouling tubeworm (Hydroides elegans) to a range of pH. In three different experiments, embryos were reared to, or past, metamorphosis in seawater equilibrated to CO2 values of about 480 (control), 980, 1,480, and 2,300 μatm resulting in pH values of around 8.1 (control), 7.9, 7.7, and 7.5, respectively. These three decreased pH conditions did not affect either embryo or larval development, but both larval calcification at the time of metamorphosis and early juvenile growth were adversely affected. During the 24-h settlement assay experiment, half of the metamorphosed larvae were unable to calcify tubes at pH 7.9 while almost no tubes were calcified at pH 7.7. Decreased ability to calcify at decreased pH may indicate that these calcifying tubeworms may be one of the highly threatened species in the future ocean.
The uptake of anthropogenic CO2 emissions by oceans has started decreasing pH and carbonate ion concentrations of seawater, a process called ocean acidification (OA). Occurring over centuries and many generations, evolutionary adaptation and epigenetic transfer will change species responses to OA over time. Trans-generational responses, via genetic selection or trans-generational phenotypic plasticity, differ depending on species and exposure time as well as differences between individuals such as gender. Males and females differ in reproductive investment and egg producing females may have less energy available for OA stress responses. By crossing eggs and sperm from the calcareous tubeworm Hydroides elegans (Haswell, 1883) raised in ambient (8.1) and low (7.8) pH environments, we observed that paternal and maternal low pH experience had opposite and additive effects on offspring. For example, when compared to offspring with both parents from ambient pH, growth rates of offspring of fathers or mothers raised in low pH were higher or lower respectively, but there was no difference when both parents were from low pH. Gender differences may result in different selection pressures for each gender. This may result in overestimates of species tolerance and missed opportunities of potentially insightful comparisons between individuals of the same species.
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