Plasticity in organic composition maintains biomechanical performance in shells of juvenile scallops exposed to altered temperature and pH conditions

Abstract

The exposure to environmental variations in pH and temperature has proven impacts on benthic ectotherms calcifiers, as evidenced by tradeoffs between physiological processes. However, how these stressors affect structure and functionality of mollusk shells has received less attention. Episodic events of upwelling of deep cold and low pH waters are well documented in eastern boundary systems and may be stressful to mollusks, impairing both physiological and biomechanical performance. These events are projected to become more intense, and extensive in time with ongoing global warming. In this study, we evaluate the independent and interactive effects of temperature and pH on the biomineral and biomechanical properties of Argopecten purpuratus scallop shells. Total organic matter in the shell mineral increased under reduced pH (~ 7.7) and control conditions (pH ~ 8.0). The periostracum layer coating the outer shell surface showed increased protein content under low pH conditions but decreasing sulfate and polysaccharides content. Reduced pH negatively impacts shell density and increases the disorder in the orientation of calcite crystals. At elevated temperatures (18 °C), shell microhardness increased. Other biomechanical properties were not affected by pH/temperature treatments. Thus, under a reduction of 0.3 pH units and low temperature, the response of A. purpuratus was a tradeoff among organic compounds (biopolymer plasticity), density, and crystal organization (mineral plasticity) to maintain shell biomechanical performance, while increased temperature ameliorated the impacts on shell hardness. Biopolymer plasticity was associated with ecophysiological performance, indicating that, under the influence of natural fluctuations in pH and temperature, energetic constraints might be critical in modulating the long-term sustainability of this compensatory mechanism.

Biomechanical Characterization of Scallop Shells Exposed to Ocean Acidification and Warming

“…These results are different from those reported previously in the compression behavior where it shows significant differences ( p < 0.05) in the elastic modulus between the pH 7.6 and 14°C group and all the others, including the control, wet condition, and compression in the thickness ( Lagos et al, 2021 ). The above indicates anisotropic behavior in compression with significantly different properties from each other.…”

“…Therefore, and considering the results obtained in the present study, it can be said that for AP it is validly mechanically modeled with a unimodular orthotropic model, where the directions of the principal stresses to which it is subjected are directly related according to its crystalline microstructure (Acevedo et al, 2010;Tippmann and Benavente, 2014;Almagro et al, 2016;Lagos et al, 2021). This is significant due to the survival mechanisms that the animal can develop under mechanical loads, allowing us to know the direction and orientation in which the shell concentrates the principal stresses.…”

“…Therefore, the numerical simulations will focus on the control group (pH 8.1 and 14°C) representing the expected behavior. On the other hand, it is interesting to compare what was obtained in tensile tests with the compression properties ( Lagos et al, 2021 ), as, in magnitude, there is a difference close to 82% (based on a relative error centered on the compression properties), which could give signs of bimodular behavior, so, focused on the fitting process in the tensile test, this factor will be evaluated.…”

“…Fitzer et al evaluated the fracture resistance of Mytilus edulis shells under the effects of climate change, in which mollusk was cultured at projected levels of pCO 2 and increased temperatures (Fitzer et al, 2015). Recent research carried out studies on juvenile AP (same samples used for the present study) measuring organic content and composition, crystallography and biomechanical properties (to compression), results that indicate significant changes in the composition of the outer part of the shell and also showed that acidification increases the orientation disorder of calcite crystals and reduces their mineral density around 20% (Lagos et al, 2021), which validates what Ramajo et al study (Ramajo et al, 2019). However, in the groups studied, the only significant differences found in mechanical properties at compression were between test directions, i.e., orthotropic anisotropy was found precluding.…”

“…8.0 to 7.8, and reaching pH 7.6 by the year 2200 ( Wolf-Gladrow et al, 1999 ). There is evidence that the Chilean coastal upwelling areas (30° South latitude) have naturally low pH (acidic) and high concentrations of dissolved carbon dioxide ( Torres and Ampuero, 2009 ; Ramajo et al, 2019 ; Ramajo et al, 2020 ; Lagos et al, 2021 ), which have been projected to be more prolonged events due to the effects of global warming in the following decades ( Bakun, 1990 ; Kim et al, 2013 ; Wang et al, 2015 ). These conditions are exposed to progressive acidification described for other coasts such as Oregon and California upwelling ecosystems ( Feely et al, 2008 ; Gruber et al, 2012 ; Kim et al, 2013 ).…”