Nanoscale Characterization of Microscopically Layered Bone in the Russian Sturgeon Pectoral Fin Spine: A 3D FIB-SEM...

Dermal bone, the earliest known form of bone, develops without a cartilage precursor and persists in extant fish species. The pectoral fin spine (PFS) is a dermal bone located at the leading edge of the pectoral fin of sturgeons, where it is exposed to loading associated with locomotion. The peripheral region and dermal osteons of the PFS both appear layered at lower magnification; however, collagen organization in load-bearing fish skeletal elements remains incompletely characterized at the nanoscale. The aim of this study is to characterize the 3D nanostructure of the layered peripheral and osteonal bone forming the PFS in Russian sturgeons using focused ion beam-scanning electron microscopy (FIB-SEM). In the dermal osteons, bone forms concentric layers around a central canal at lower magnification, and at the nanoscale, the calcified collagen fibrils within these layers have preferential orientations that change in a clockwise-anticlockwise fanning pattern, consistent with lamellar bone. In contrast, the examined peripheral bone, which also appears layered at low magnification, is composed mainly of unidirectional calcified collagen fibrils aligned with the long axis of the PFS. Within the examined peripheral volumes, no comparable nanoscale lamellar pattern was detected, and the predominant fibril organization was consistent with parallel-fibered bone. Groups of voids associated with unidentified fibrillar material were also observed in the examined peripheral volumes; the voids were oriented approximately normal to the long axis of the PFS. We conclude that regions appearing layered at lower magnification can differ markedly at the nanoscale, and that the lamellar organization seen in dermal osteons raises questions about its evolutionary origin.