Diversity of dermal denticle structure in sharks: Skin surface roughness and three‐dimensional morphology

Abstract

Shark skin is covered with numerous placoid scales or dermal denticles. While previous research has used scanning electron microscopy and histology to demonstrate that denticles vary both around the body of a shark and among species, no previous study has quantified three-dimensional (3D) denticle structure and surface roughness to provide a quantitative analysis of skin surface texture. We quantified differences in denticle shape and size on the skin of three individual smooth dogfish sharks (Mustelus canis) using micro-CT scanning, gel-based surface profilometry, and histology. On each smooth dogfish, we imaged between 8 and 20 distinct areas on the body and fins, and obtained further comparative skin surface data from leopard, Atlantic sharpnose, shortfin mako, spiny dogfish, gulper, angel, and white sharks. We generated 3D images of individual denticles and measured denticle volume, surface area, and crown angle from the micro-CT scans. Surface profilometry was used to quantify metrology variables such as roughness, skew, kurtosis, and the height and spacing of surface features. These measurements confirmed that denticles on different body areas of smooth dogfish varied widely in size, shape, and spacing. Denticles near the snout are smooth, paver-like, and large relative to denticles on the body. Body denticles on smooth dogfish generally have between one and three distinct ridges, a diamond-like surface shape, and a dorsoventral gradient in spacing and roughness. Ridges were spaced on average 56 µm apart, and had a mean height of 6.5 µm, comparable to denticles from shortfin mako sharks, and with narrower spacing and lower heights than other species measured. We observed considerable variation in denticle structure among regions on the pectoral, dorsal, and caudal fins, including a leading-to-trailing edge gradient in roughness for each region. Surface roughness in smooth dogfish varied around the body from 3 to 42 microns.

Microstructural morphology of dermal and oral denticles of the sharpnose sevengill shark Heptranchias perlo (Elasmobranchii: Hexanchidae), a deep‐water species

“…In summary, our results showed that, as seen in other species (e.g., Ankhelyi et al, ), the denticles vary considerably throughout the body, including the oral cavity. Considering the great potential of the use of denticles as a tool for taxonomic and ecological studies (e.g., Dillon et al, ; Mello et al, ), understanding how such variation is species‐specific is essential, especially because the intraspecific variation in dermal and oral denticles were body‐region‐dependent.…”

“…However, by observing other regions, it was possible to identify specific functional morphotypes, such as abrasion strength found on the tip of the nose, probably providing protection during feeding. This morphotype is commonly observed in other sharks in these regions (e.g., Mustelus canis, Ankhelyi et al, 2018). Similarly, the denticles found in the dorsal anterior region were similar to the described ridged abrasion strength denticles (Dillon et al, 2017).…”

“…Some particularities of the denticles that make them interesting tools include: (a) their morphological aspects (i.e., shape, size, and arrangement) are highly variable intra and interspecifically; (b) they are correlated with shark ecology; (c) are very abundant across the body of sharks, including oral regions and nictitating membrane; and (d) are continually exchanged (e.g., Dillon et al, 2017;Poscai et al, 2017;Rangel et al, 2017). Although recent studies have addressed extensively about morphology, taxonomy, and function of denticles (e.g., Dillon et al, 2017), more studies are needed considering both the high shark diversity (~500 living species; Weigmann, 2016) and intra and interspecifically variability of denticles across the body and oral cavity (e.g., Ankhelyi, Wainwright, & Lauder, 2018;Dillon et al, 2017;Rangel, Salmon, Poscai, Kfoury Jr., & Rici, 2019). Such a taxonomic tool seems to be especially interesting to explore areas where research is more difficult to perform such as in deep-water shark communities, despite its limited application to species and genus level identification (Dillon et al, 2017).…”

Ontogenetic scaling patterns of lizard skin surface structure as revealed by gel‐based stereo‐profilometry

“…While imaging and quantifying the complexity of biological surface structures can be accomplished by various methods, such as atomic force microscopy (Huber et al 2005), micro-computed tomography (Broeckhoven et al 2017) and scanning electron microscopy (Russell & Johnson, 2014;Riedel et al 2015), these techniques often require extensive specimen preparation and/or long image acquisition times, and are thus not well suited for the high-throughput analysis of large numbers of specimens in a non-destructive manner. In contrast, gel-based stereoprofilometry (Johnson & Adelson, 2009;Li & Adelson, 2013) has recently proved to be an exceptionally useful technique for the rapid 3D structural characterization of biological surfaces without any specimen preparation, permitting 3D visualization in situ and even in vivo Wainwright et al 2017;Ankhelyi et al 2018;. Inspired by these previous studies, which have primarily focused on the structural characterization of fish scales, we here demonstrated that gel-based stereo-profilometry is also an effective tool for visualizing and quantifying the scaled surfaces of squamates.…”

“…; Ankhelyi et al. ; Wainwright & Lauder, ). Inspired by these previous studies, which have primarily focused on the structural characterization of fish scales, we here demonstrated that gel‐based stereo‐profilometry is also an effective tool for visualizing and quantifying the scaled surfaces of squamates.…”