The unique configuration of dentinal tubules and hard tissue architecture within the narwhal tusk supports a new hypothesis for function. Two freshly harvested male tusks, examined under scanning electron microscopy, reveal dentinal tubules that are open and extend continuously from the pulp to the external environment. Approximately 1 tubule opening every 200 µm2, ranging from 0.1-4 µm are visible on the pulpal wall. Analogous surface lumena are visible within a 10-20 µm layer of diatoms and algae that cover the surface. Brannstrom’s hydrodynamic theory identifies pain sensitivity in mammals that have tubule communication of pathologic origin from the tooth or root surface to the pulp. With over 106 tubules in an eight-foot tusk, potential exists for the tusk to be used as a hydrodynamic sensor to detect fluid flow responsive to gradients of salinity, temperature and pressure. Chemical and mechanical properties of the tusk also indicate unusual functional adaptation. Cross-sections of one tusk near the tip (#1), ј length from the tip (#2), and near the base (#3), were dry polished and mapped by Fourier-transform infrared reflectance microspectroscopy (FTIR-RM) at 100x100 µm to 200x200 µm spatial resolution and by nanoindentation at 200x100 µm spatial resolution. FTIR-RM analysis showed higher mineral to collagen ratios (MCR) near the dentin-pulp interface and decreasing toward the cementum interface in #1 and #2, with non significant difference in #3. Mechanical indices of hardness and Young’s Modulus were highest at the dentin-pulp interface and decreasing outward toward the cementum in all sections. All three properties declined from tip to base, with modulus demonstrating dramatic decline moving from pulp to the outer surface. The outer layers being less mineralized and more flexible than the inner layers in sections closer to the tip indicate unusual resilience and flexibility of the tusk and suggest important evolutionary functional adaptation.