Ocean acidification reduces hardness and stiffness of the Portuguese oyster shell with impaired microstructure: a hierarchical analysis

Abstract

Abstract. The rapidly intensifying process of ocean acidification (OA) due to anthropogenic CO2 is not only depleting carbonate ions necessary for calcification but also causing acidosis and disrupting internal pH homeostasis in several marine organisms. These negative consequences of OA on marine calcifiers, i.e. oyster species, have been very well documented in recent studies; however, the consequences of reduced or impaired calcification on the end-product, shells or skeletons, still remain one of the major research gaps. Shells produced by marine organisms under OA are expected to show signs of dissolution, disorganized microstructure and reduced mechanical properties. To bridge this knowledge gap and to test the above hypothesis, we investigated the effect of OA on juvenile shells of the commercially important oyster species, Magallana angulata, at ecologically and climatically relevant OA levels (using pH 8.1, 7.8, 7.5, 7.2). In lower pH conditions, a drop of shell hardness and stiffness was revealed by nanoindentation tests, while an evident porous internal microstructure was detected by scanning electron microscopy. Crystallographic orientation, on the other hand, showed no significant difference with decreasing pH using electron back-scattered diffraction (EBSD). These results indicate the porous internal microstructure may be the cause of the reduction in shell hardness and stiffness. The overall decrease of shell density observed from micro-computed tomography analysis indicates the porous internal microstructure may run through the shell, thus inevitably limiting the effectiveness of the shell's defensive function. This study shows the potential deterioration of oyster shells induced by OA, especially in their early life stage. This knowledge is critical to estimate the survival and production of edible oysters in the future ocean.

Understanding decay in marine calcifiers: Micro‐CT analysis of skeletal structures provides insight into the impacts of a changing climate in marine ecosystems

“…For example, a 2D cross-section of the shortspined sea urchin Heliocidaris erythrogramma from a 3D tomogram displays a highly connected and complex pore space (Johnson et al, 2020), similar to that of Porites cylindrica (Video S1), which would make it amenable to MIS analysis. The SEM images of a Portuguese oyster shell Magallana angulata presented by Meng et al (2018) indicate that the combination of pores and fissures in this case would require jointly applying PSD and MIS analysis on different regions of interest. But in both instances, SEM was used to describe the widening of more spaces.…”

“…Measurement is highly dependent upon where the 2D image is taken. Destructive Tribollet, Decherf, Hutchings, and Peyrot-Clausade (2002), Milner, Langer, Grelaud, and Ziveri (2016), Bylenga, Cummings, and Ryan (2017), Meng et al (2018) and Leggat et al (2019) Nuclear magnetic resonance imaging Samples are saturated with water and held inside a constant magnetic field.…”

“…density). Historically, µCT imaging of marine calcifiers has employed binary segmentation, in which a single greyscale intensity threshold is used to distinguish between solid CaCO 3 and air (DeCarlo, 2017; Gooday et al, 2018;Meng et al, 2018;Roche et al, 2010;Silbiger et al, 2016). This threshold can be manipulated to produce the most realistic operator-perceived segmentation (Veal, Holmes, Nunez, Hoegh-Guldberg, & Osborn, 2010) or may be calibrated based on objective measures such as density measured by Archimedean principles (Silbiger et al, 2016) or using Otsu's thresholding (Otsu, 1979) which can automatically segment images based on maximizing variance between the classes of voxels (e.g.…”

“…It has been employed for very high-resolution (i.e. single microns) studies of a range of calcifying taxa including pteropods, gastropods, rhodophytes, bivalves and annelids, quantifying density, shell thickness and volume in the context of biomechanical change (Chatzinikolaou, Grigoriou, Keklikoglou, Faulwetter, & Papageorgiou, 2016;Li et al, 2014;Meng et al, 2018;Oakes & Sessa, 2019). But a lack of advanced analytical techniques to complement this means that certain features of carbonate structures, such as pore space morphology, are still predominantly measured using 2D microscopy such as SEM (Byrne & Fitzer, 2019;Li et al, 2014;Meng et al, 2018).…”

“…A decrease in exoskeletal durability and strength has broad consequences for ecosystem structure and function. For pelagic and benthic calcifiers, alterations to their shell structure will affect their ability to capture light, and protect themselves from predation and UV damage (Enríquez, Méndez Eugenio, Hoegh-Guldberg, & Iglesias-Prieto, 2017;Meng et al, 2018;Monteiro et al, 2016;Orr et al, 2005). Reef-building organisms will suffer a loss of structural stability, compromising key ecosystem services such as commercial fishing and coastal protection (Fantazzini et al, 2015;Graham & Nash, 2013;Meng et al, 2018).…”