A new experimentally testable hypothesis is advanced for the mechanosensory transduction mechanism by which communicating osteocytes sense the very small in vivo strains in the calcified matrix components of bone. We propose that the osteocytes, although not responsive to substantial fluid pressures, can be stimulated by relatively small fluid shear stresses acting on the membranes of their osteocytic processes. Biot's porous media theory is used to relate the combined axial and bending loads applied to a whole bone to the flow past the osteocytic processes in their canaliculi. In this theory, the bone pores of interest are the proteoglycan filled fluid annuli that surround the osteocytic processes in the canaliculi. We show that previously predicted fluid pore pressure relaxation times were a hundred-fold too short for the lacunar-canalicular porosity because they neglected the fluid drag associated with proteoglycan matrix on the surface membrane of the osteocyte and its cell processes. The recent theory developed in Tsay and Weinbaum [J. Fluid Mech. 226, 125-148 (1991)] for flow through cross-linked fiber filled channels is used to model the flow through this proteoglycan matrix. The predicted pore relaxation time, 1-2 s, closely corresponds to the times measured by Salzstein and Pollack [J. Biomechanics 20, 271-280 (1987)]. Furthermore, using this model, the magnitude of the predicted fluid induced shear stresses, 8-30 dyn cm-2, is shown to be similar to the fluid shear stresses measured in osteoblasts and other cells in which an intracellular Ca2+ shear stress response had been observed. This model is also used, in conjunction with anatomical data and the pore fluid pressure relaxation time data, to show that the spacing between the fibers is approximately 7 nm. The result is consistent with the notion that the canalicular pore space is filled with glycosaminoglycans that are ordered by albumin according to the model of Michel [J. Physiol. 404, 1-29 (1988)]. The new hypothesis is also shown to be consistent with the experiments of McLeod et al. [J. Biomechanics (submitted)] which suggest that high-frequency low-amplitude postural strains can maintain and even increase bone mass.