Significance: A fundamental paradigm of bone biology is that the remodeling process—by which bones detect and repair damage—is orchestrated by osteocytes. The bones of most extant fish, however, lack these cells and should be unable to repair damage in their bones. We provide evidence for intense remodeling in the anosteocytic bone of billfishes, such as swordfish and marlin. Our observations challenge the central axiom that osteocytes alone are responsible for remodeling, suggesting alternate mechanisms in bone physiology and/or variation in the roles of bone cells. In addition, billfish bone exhibits an array of striking material properties that distinguish it from mammalian bone despite having similar composition, underlining that skeletal biology concepts are limiting when based on mammalian tissues alone.

SUMMARY The histological diversity of the skeletal tissues of fishes is impressive compared with that of other vertebrate groups, yet our understanding of the functional consequences of this diversity is limited. In particular, although it has been known since the mid-1800s that a large number of fish species possess acellular bones, the mechanical advantages and consequences of this structural characteristic – and therefore the nature of the evolution of this feature – remain unclear. Although several studies have examined the material properties of fish bone, these have used a variety of techniques and there have been no direct contrasts of acellular and cellular bone. We report on a comparison of the structural and mechanical properties of the ribs and opercula between two freshwater fish – the common carp Cyprinus carpio (a fish with cellular bone) and the tilapia Oreochromis aureus (a fish with acellular bone). We used light microscopy to show that the bones in both fish species exhibit poor blood supply and possess discrete tissue zones, with visible layering suggesting differences in the underlying collagen architecture. We performed identical micromechanical testing protocols on samples of the two bone types to determine the mechanical properties of the bone material of opercula and ribs. Our data support the consensus of literature values, indicating that Young’s moduli of cellular and acellular bones are in the same range, and lower than Young’s moduli of the bones of mammals and birds. Despite these similarities in mechanical properties between the bone tissues of the fish species tested here, cellular bone had significantly lower mineral content than acellular bone; furthermore, the percentage ash content and bone mineral density values (derived from micro-CT scans) show that the bone of these fishes is less mineralized than amniote bone. Although we cannot generalize from our data to the numerous remaining teleost species, the results presented here suggest that while cellular and acellular fish bone may perform similarly from a mechanical standpoint, there are previously unappreciated differences in the structure and composition of these bone types.