Renal uroliths (concrements) of calcium phosphate have long been known to exist in both growing and mature (non-growing) Nautilus specimens, but to date no evidence-based explanation for their existence has been available. The currently favored speculation is that they function as a calcium reserve for shell and septal calcification. Here we present new observational and experimental data that are consistent with the hypothesis that they serve as a mineral/ion reserve, allowing short-term (<1 day) addition of ionized calcium and phosphorus to blood and other body fluids, in a way analogous to that of vertebrate bone. In both in-ocean experiments and during long-term observation of captive nautiluses, concrements disappear during two different, energy-intensive activities involving removal of anions and cations from newly secreted cameral liquid in the chamber formation cycle, and during dives to depths requiring high osmotic pressures within the canaliculi of the siphuncular epithelium to keep previously emptied chambers from flooding due to suddenly increased ambient hydrostatic pressure. New concrements reappear at other points in the chamber formation cycle and when normal living depth is restored. The use of concrements as an ion reserve and the Cambrian ancestry of nautiloids indicate that Nautilus may exemplify a solution to the problem of energy supply in newly evolved swimmers of the Cambrian radiation independent of that seen in fish.