Stiffness without mineral: material properties and biochemical components of jaws and chondrocrania in the Elasmobranchii (sharks, skates, and rays)

Abstract

26Chondrichthyians (sharks, ratfish, and rays) can function at extremes (growing big, swimming 27 fast, and eating hard-prey) suggesting their skeletons are experiencing loading regimes equal to 28 or greater than those of other fishes. In most vertebrates, cartilage is a soft connective tissue 29 serving two purposes; a low-friction bearing surface and contour filler; however, cartilaginous 30 fishes maintain a skeleton made of cartilage throughout life. We examined material properties 31 and biochemical components of cartilage from the jaws and/or chondrocranium of seven species 32 of shark. For each species cylindrical plugs were drilled from the specimen, mineralized tesserae 33were removed, and plugs tested in compression to ten percent of initial thickness (ε=0.10) at 34 2mm/sec. Stiffness and strength varied significantly among species and in both cases the 35 chondrocranial properties were greater than those of the jaws. After materials testing, cartilage 36 plugs were lyophilized to obtain water content; then collagen and proteoglycan was measured 37 with hydroxyproline and DMMB assays, respectively. Water content was greatest in the 38 chondrocranial cartilage while collagen content was consistent between the jaws and 39 chondrocrania. However, proteoglycan content was greater in the jaw cartilage. The average 40 values for water and proteoglycan content were consistent with mammalian cartilage, while 41 collagen content was much lower than mammalian cartilage. Material properties and 42 biochemical components were also similar to the mineralized cartilage found in elasmobranch 43 vertebral cartilage.

Mechanical properties of the hyomandibula in four shark species

“…The apparatus was placed into elasmobranch ringer's solution (Forster et al, ) for at least 30 min to allow the putty to set. Once set, the putty had an elastic modulus of 3.19 GPa, which is three orders of magnitude higher than the modulus of articular cartilage and about one order of magnitude higher than that of previously tested mineralized shark cartilage (Korhonen et al, ; Jin and Lewis, ; Stolz et al, ; Porter et al, 2006, 2013; Macesic and Summers, ; Ferrara et al, ; Huber et al, ; Liu et al, ; ). The hyomandibula was then placed in the materials testing machine so the discs were parallel with the compression platens and the hyomandibula could be loaded along the longitudinal axis (Fig.…”

“…This strategy of hypermineralization is reminiscent of the thick outer layers and even trabeculation of the jaw cartilages in hard prey crushing stingrays and sharks (Summers, ; Summers et al, ). Three studies have reported values for the stiffness of unmineralized cartilage (), with one finding values ranging from 20 to 776 MPa (Porter et al, ), one ranging from 0.15 to 5.56 MPa (Liu et al, ), and the third ranging from 9.97 to 35.90 MPa (Ferrara et al, ). Though these values for stiffness range widely, many of the values for hyomandibular cartilages fall above those for unmineralized cartilage, and most of the stiffness is likely due to the level of mineralization.…”

“…These higher degrees of stiffness and differing Poisson's ratios were seen even though uniform cubes of bone were used for compression testing. The difference between axes of compression is due to the sub‐structural properties of the bone, such as the orientation of the mineralized collagen fibril bundles (Weiner and Wagner, ; Shahar et al, ) Two studies so far have measured stiffness from uniform blocks of shark cartilage (Porter et al, ; Liu et al, ). Both studies measured the compressive stiffness of unmineralized cartilage along one axis, and one additionally measured the stiffness of tessellated cartilage along two axes (Liu et al, ).…”