Nacre tablet thickness records formation temperature in modern and fossil shells

Nacre, the iridescent outer lining of pearls and inner lining of many mollusk shells, is composed of periodic, parallel, organic sheets alternating with aragonite (CaCO_3) tablet layers. Nacre tablet thickness (TT) generates both nacre's iridescence and its remarkable resistance to fracture. Despite extensive studies on how nacre forms, the mechanisms controlling TT remain unknown, even though they determine the most conspicuous of nacre's characteristics, visible even to the naked eye. Thermodynamics predicts that temperature (T) will affect both physical and chemical components of biomineralized skeletons. The chemical composition of biominerals is well-established to record environmental parameters, and has therefore been extensively used in paleoclimate studies. The physical structure, however, has been hypothesized but never directly demonstrated to depend on the environment. Here we observe that the physical TT in nacre from modern and fossil shallow-water shells of the bivalves Pinna and Atrina correlates with T as measured by the carbonate clumped isotope thermometer. Based on the observed TT vs. T correlation, we anticipate that TT will be used as a paleothermometer, useful to estimate paleotemperature in shallow-water paleoenvironments. Here we successfully test the proposed new nacre TT thermometer on two Jurassic Pinna shells. The increase of TT with T is consistent with greater aragonite growth rate at higher T, and with greater metabolic rate at higher T. Thus, it reveals a complex, T-dependent biophysical mechanism for nacre formation

A Molecular-Scale Understanding of Misorientation Toughening in Corals and Seashells.

peer reviewedBiominerals are organic-mineral composites formed by living organisms. They are the hardest and toughest tissues in those organisms, are often polycrystalline, and their mesostructure (which includes nano- and microscale crystallite size, shape, arrangement, and orientation) can vary dramatically. Marine biominerals may be aragonite, vaterite, or calcite, all calcium carbonate (CaCO3 ) polymorphs, differing in crystal structure. Unexpectedly, diverse CaCO3 biominerals such as coral skeletons and nacre share a similar characteristic: Adjacent crystals are slightly misoriented. This observation is documented quantitatively at the micro- and nanoscales, using polarization-dependent imaging contrast mapping (PIC mapping), and the slight misorientations are consistently between 1° and 40°. Nanoindentation shows that both polycrystalline biominerals and abiotic synthetic spherulites are tougher than single-crystalline geologic aragonite. Molecular dynamics (MD) simulations of bicrystals at the molecular scale reveal that aragonite, vaterite, and calcite exhibit toughness maxima when the bicrystals are misoriented by 10°, 20°, and 30°, respectively, demonstrating that slight misorientation alone can increase fracture toughness. Slight-misorientation-toughening can be harnessed for synthesis of bioinspired materials that only require one material, are not limited to specific top-down architecture, and are easily achieved by self-assembly of organic molecules (e.g., aspirin, chocolate), polymers, metals, and ceramics well beyond biominerals

Mollusk Shell Nacre Ultrastructure Correlates with Environmental Temperature and Pressure

Nacre, or mother-of-pearl, the tough, iridescent biomineral lining the inner side of some mollusk shells, has alternating biogenic aragonite (calcium carbonate, CaCO₃) tablet layers and organic sheets. Nacre has been common in the shells of mollusks since the Ordovician (450 million years ago) and is abundant and well-preserved in the fossil record, e.g., in ammonites. Therefore, if any measurable physical aspect of the nacre structure was correlated with environmental temperatures, one could obtain a structural paleothermometer of ancient climates. Using X-ray absorption near-edge structure (XANES) spectroscopy, Photoelectron emission spectromicroscopy (PEEM), and X-ray linear dichroism we acquired polarization-dependent imaging contrast (PIC) maps of pristine nacre in cross-section. The new PIC-map data reveal that the nacre ultrastructure (nacre tablet width, thickness, and angle spread) is species-specific in at least eight mollusk species from completely different environments: <i>Nautilus pompilius</i>, <i>Haliotis iris</i>, <i>Haliotis rufescens</i>, <i>Bathymodiolus azoricus</i>, <i>Atrina rigida</i>, <i>Lasmigona complanata</i>, <i>Pinctada margaritifera</i>, and <i>Mytilus californianus</i>. Nacre species-specificity is interpreted as a result of adaptation to diverging environments. We found strong correlation between nacre crystal misorientations and environmental temperature, further supported by secondary ion mass spectrometry measurements of <i>in situ</i> δ¹⁸O in the nacre of one shell. This has far-reaching implications: nacre texture may be used as a paleothermometer of ancient climate, spanning 450 million years of Earth's history

Mollusk Shell Nacre Ultrastructure Correlates with Environmental Temperature and Pressure

Nacre, or mother-of-pearl, the tough, iridescent biomineral lining the inner side of some mollusk shells, has alternating biogenic aragonite (calcium carbonate, CaCO₃) tablet layers and organic sheets. Nacre has been common in the shells of mollusks since the Ordovician (450 million years ago) and is abundant and well-preserved in the fossil record, e.g., in ammonites. Therefore, if any measurable physical aspect of the nacre structure was correlated with environmental temperatures, one could obtain a structural paleothermometer of ancient climates. Using X-ray absorption near-edge structure (XANES) spectroscopy, Photoelectron emission spectromicroscopy (PEEM), and X-ray linear dichroism we acquired polarization-dependent imaging contrast (PIC) maps of pristine nacre in cross-section. The new PIC-map data reveal that the nacre ultrastructure (nacre tablet width, thickness, and angle spread) is species-specific in at least eight mollusk species from completely different environments: <i>Nautilus pompilius</i>, <i>Haliotis iris</i>, <i>Haliotis rufescens</i>, <i>Bathymodiolus azoricus</i>, <i>Atrina rigida</i>, <i>Lasmigona complanata</i>, <i>Pinctada margaritifera</i>, and <i>Mytilus californianus</i>. Nacre species-specificity is interpreted as a result of adaptation to diverging environments. We found strong correlation between nacre crystal misorientations and environmental temperature, further supported by secondary ion mass spectrometry measurements of <i>in situ</i> δ¹⁸O in the nacre of one shell. This has far-reaching implications: nacre texture may be used as a paleothermometer of ancient climate, spanning 450 million years of Earth's history

Spherulitic Growth of Coral Skeletons and Synthetic Aragonite: Nature’s Three-Dimensional Printing

Coral skeletons were long assumed to have a spherulitic structure, that is, a radial distribution of acicular aragonite (CaCO₃) crystals with their <i>c</i>-axes radiating from series of points, termed centers of calcification (CoCs). This assumption was based on morphology alone, not on crystallography. Here we measure the orientation of crystals and nanocrystals and confirm that corals grow their skeletons in bundles of aragonite crystals, with their <i>c</i>-axes and long axes oriented radially and at an angle from the CoCs, thus precisely as expected for feather-like or “plumose” spherulites. Furthermore, we find that in both synthetic and coral aragonite spherulites at the nanoscale adjacent crystals have similar but not identical orientations, thus demonstrating by direct observation that even at nanoscale the mechanism of spherulite formation is non-crystallographic branching (NCB), as predicted by theory. Finally, synthetic aragonite spherulites and coral skeletons have similar angle spreads, and angular distances of adjacent crystals, further confirming that coral skeletons are spherulites. This is important because aragonite grows anisotropically, 10 times faster along the <i>c</i>-axis than along the <i>a</i>-axis direction, and spherulites fill space with crystals growing almost exclusively along the <i>c</i>-axis, thus they can fill space faster than any other aragonite growth geometry, and create isotropic materials from anisotropic crystals. Greater space filling rate and isotropic mechanical behavior are key to the skeleton’s supporting function and therefore to its evolutionary success. In this sense, spherulitic growth is Nature’s 3D printing

Parrotfish Teeth: Stiff Biominerals Whose Microstructure Makes Them Tough and Abrasion-Resistant To Bite Stony Corals

Parrotfish (<i>Scaridae</i>) feed by biting stony corals. To investigate how their teeth endure the associated contact stresses, we examine the chemical composition, nano- and microscale structure, and the mechanical properties of the steephead parrotfish <i>Chlorurus microrhinos</i> tooth. Its enameloid is a fluorapatite (Ca₅(PO₄)₃F) biomineral with outstanding mechanical characteristics: the mean elastic modulus is 124 GPa, and the mean hardness near the biting surface is 7.3 GPa, making this one of the stiffest and hardest biominerals measured; the mean indentation yield strength is above 6 GPa, and the mean fracture toughness is ∼2.5 MPa·m^1/2, relatively high for a highly mineralized material. This combination of properties results in high abrasion resistance. Fluorapatite X-ray absorption spectroscopy exhibits linear dichroism at the Ca L-edge, an effect that makes peak intensities vary with crystal orientation, under linearly polarized X-ray illumination. This observation enables polarization-dependent imaging contrast mapping of apatite, a method to quantitatively measure and display nanocrystal orientations in large, pristine arrays of nano- and microcrystalline structures. Parrotfish enameloid consists of 100 nm-wide, microns long crystals co-oriented and assembled into bundles interwoven as the warp and the weave in fabric and therefore termed fibers here. These fibers gradually decrease in average diameter from 5 μm at the back to 2 μm at the tip of the tooth. Intriguingly, this size decrease is spatially correlated with an increase in hardness