Temperature-induced microstructural changes in shells of laboratory-grown Arctica islandica (Bivalvia)

Abstract

Bivalve shells are increasingly used as archives for high-resolution paleoclimate analyses. However, there is still an urgent need for quantitative temperature proxies that work without knowledge of the water chemistry–as is required for δ18O-based paleothermometry–and can better withstand diagenetic overprint. Recently, microstructural properties have been identified as a potential candidate fulfilling these requirements. So far, only few different microstructure categories (nacreous, prismatic and crossed-lamellar) of some short-lived species have been studied in detail, and in all such studies, the size and/or shape of individual biomineral units was found to increase with water temperature. Here, we explore whether the same applies to properties of the crossed-acicular microstructure in the hinge plate of Arctica islandica, the microstructurally most uniform shell portion in this species. In order to focus solely on the effect of temperature on microstructural properties, this study uses bivalves that grew their shells under controlled temperature conditions (1, 3, 6, 9, 12 and 15°C) in the laboratory. With increasing temperature, the size of the largest individual biomineral units and the relative proportion of shell occupied by the crystalline phase increased. The size of the largest pores, a specific microstructural feature of A. islandica, whose potential role in biomineralization is discussed here, increased exponentially with culturing temperature. This study employs scanning electron microscopy in combination with automated image processing software, including an innovative machine learning–based image segmentation method. The new method greatly facilitates the recognition of microstructural entities and enables a faster and more reliable microstructural analysis than previously used techniques. Results of this study establish the new microstructural temperature proxy in the crossed-acicular microstructures of A. islandica and point to an overarching control mechanism of temperature on the micrometer-scale architecture of bivalve shells across species boundaries.

Coupling Mineralogy and Oxygen Isotopes to Seasonal Environmental Shifts Recorded in Modern Freshwater Pearl Nacre From Kentucky Lake

“…In culturing experiments, Höche et al. (2021) also observe shifts in Arctica islandica microstructure in the non‐nacreous hinge plate region of the shell as a function of increasing temperature. Beyond changes in tablet morphology and orientation with temperature, little else has been explored to tie the micron‐ to atomic‐scale mineralogy and crystal structures of nacre aragonite to specific shifts in surrounding environmental and growth conditions, as has been previously examined in coral aragonite (DeCarlo et al., 2017; Farfan et al., 2018).…”

Microstructural Mapping of Arctica islandica Shells Reveals Environmental and Physiological Controls on Biomineral Size

“…This is typically accomplished by slight etching of the BMUs and/or removal of the intercrystalline organic matrices, e.g., by immersion of the shells in weak acids, bleach or hydrogen peroxide (Crippa et al, 2016). This treatment, however, evokes a violent reaction (Lavkulich and Wiens, 1970), alters the original BMU shape (Höche et al, 2021a) and sometimes affects different materials of the shell heterogeneously. To overcome these problems, an ultrafine chemo-mechanical polishing step was instead employed in this study: shell slabs were polished for 10 minutes on a rotational lap (Buehler MetaServ 2000) at 50 rpm using a Buehler MasterTex polishing cloth and Buehler MasterMet polishing suspension.…”

“…As a previous study revealed a statistically significant relationship between the BMU size in the hinge plate of laboratory grown specimens and temperature (Höche et al, 2021a), the same shell portions were investigated here (953 images; Table 1). For comparison of BMU data in different contemporaneous portions of the shell, the outer shell layer (OSL) of the ventral margin was also studied (241 images; Table 1).…”

“…Furthermore, temperature reconstructions based on the shell microstructure might be less affected by other environmental factors than conventional proxies, such as the δ 18 O shell , which require knowledge of the δ 18 O water signature or salinity. Microstructural properties of the long-lived Arctica islandica have gained particular interest (Milano et al, 2017a;Höche et al, 2021a), because this bivalve species not only forms distinct annual shell growth patterns, but also attains a lifespan of several hundred years (Thompson et al, 1980a;Schöne et al, 2005b;Wanamaker et al, 2008;Butler et al, 2013) and has a broad biogeographic distribution in the northern North Atlantic (Dahlgren et al, 2000;Schöne, 2013), prerequisites for long-term and high-resolution paleoclimate reconstructions in a climatologically highly relevant part of the global ocean.…”

“…According to recent laboratory experiments the size of BMUs of A. islandica shells correlates with the water temperature (Höche et al, 2021a). However, it remains unclear whether the same relationship exists in naturally grown individuals permitting temperature reconstructions from microstructural properties.…”