Biominerals formed by animals provide skeletal support and many other functions. They were previously shown to grow by aggregation of amorphous nanoparticles but never to grow ion-by-ion from solution, which is a common growth mechanism for abiotic crystals. We analyze vaterite (CaCO3) multicrystalline spicules from the solitary tunicate Herdmania momus, with polarization-dependent imaging contrast (PIC)-mapping and scanning and aberration-corrected transmission electron microscopies. The first fully quantitative PIC-mapping data, presented here, measured 0-30°angle spreads between immediately adjacent crystals. Such narrowly distributed crystal orientations demonstrate that crystallinity does not propagate from one crystal to another (0°angle spreads), nor that new crystals with random orientation (90°) nucleate. There are no organic layers at the interface between crystals; hence, a new, unknown growth mechanism must be invoked, with crystal nucleation constrained within 30°. Two observations are consistent with crystal growth from solution: vaterite microcrystals express crystal faces and are smooth at the nanoscale after cryo-fracture. The observation of 30° angle spreads, lack of interfacial organic layers, and smooth fracture figures broadens the range of known biomineralization mechanisms and may inspire novel synthetic crystal growth strategies. Spherulitic growth from solution is one possible mechanism consistent with all these observations.

Nacre, the iridescent outer lining of pearls and inner lining of many mollusk shells, is composed of periodic, parallel, organic sheets alternating with aragonite (CaCO3) 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.