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. 2019 May 24;4(2):38.
doi: 10.3390/biomimetics4020038.

Dermal Denticles of Three Slowly Swimming Shark Species: Microscopy and Flow Visualization

Katrine Feld  1 , Anne Noer Kolborg  2 , Camilla Marie Nyborg  3 , Mirko Salewski  4 , John Fleng Steffensen  5 , Kirstine Berg-Sørensen  6
Affiliations

Dermal Denticles of Three Slowly Swimming Shark Species: Microscopy and Flow Visualization

Katrine Feld et al. Biomimetics (Basel). .

Abstract

Shark skin has for many years inspired engineers to produce biomimetic structures reducing surface drag or acting as an anti-fouling layer. Both effects are presumed to be consequences of the structure of shark skin that is composed of arrays of so-called dermal denticles. However, the understanding of the full functional role of the dermal denticles is still a topic of research. We report optical microscopy and scanning electron microscopy of dermal denticles from three slowly swimming shark species for which the functional role of the dermal denticles is suggested as one of defense (possibly understood as anti-fouling) and/or abrasion strength. The three species are Greenland shark (Somnosius microcephalus), small-spotted catshark (Scyliorhinus canicula) and spiny dogfish (Squalus acanthias). Samples were taken at over 30 different positions on the bodies of the sharks. In addition, we demonstrate that the flow pattern near natural shark skin can be measured by micro-PIV (particle image velocimetry). The microfluidic experiments are complemented by numerical flow simulations. Both visualize unsteady flow, small eddies, and recirculation bubbles behind the natural dermal denticles.

Keywords: micro-PIV; microfluidics; shark skin.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
(Color online) Microscope images of denticles of the small-spotted catshark (male, TL 72 cm). All scalebars are 1 mm. Top left image with the longest measured denticles from the back of the body, area b10 in Figure S1. The top right image shows smaller ribbed denticles from the second dorsal fin (area here denoted d4). A more random packing and direction of denticles is seen in the area behind the gills (g2), as indicated by the image in the bottom left. The last image shows denticles from the tip of the pelvic fin (area denoted p8) which are very smooth, almost drop-shaped, and transparent. The sketch in the middle is copyright Marc Dando and reprinted with his permission.
Figure 2
Figure 2
(Color online) SEM images of denticles of the Greenland shark (female, TL 470 cm) from positions n1, b3, c2 and p6 in Figure S1. Scalebars are 1 mm (n1, b3, p6) and 500 μm (c2). In area n1, the nose of the Greenland shark, a very different denticle structure than on the rest of the body is observed. On the top right of this image of area n1, a denticle that appears worn down is seen. In the area b3, it appears as if the directions of the tip of the denticles is somewhat random, whereas in other parts of the body, the denticles tend to point into the same direction, towards the tail. The central sketch of the shark is copyright Kirsten Hjørne and reprinted with her permission.
Figure 3
Figure 3
(Color online) Scheme showing the dermal denticles in different areas of the spiny dogfish (female, TL 76 cm). The SEM pictures are from top left to bottom right respectively showing dermal denticles from; the nose (n1), the caudal fin (c1), the pectoral fin (p2) and at the back of the body (b11). All scale bars are 1 mm. The central illustration of the shark is copyright Marc Dando and reprinted with his permission.
Figure 4
Figure 4
Results of micro-PIV measurements in three layers above a dermal denticle in the b1 area of the dogfish (female, TL 99 cm). In all images, the size of the area visualized is 580 μm in width and 450 μm in height. To illustrate the position of the denticle, a single denticle is extracted from an SEM image from the b1 area, scaled and overlaid with the image extracted from the PIV processing software. Positions of neighboring denticles correspond to white areas with no flow field. Part (a) illustrates both the structure of the denticle as seen from above and the flow around it, very close to the skin. The local flowspeed is indicated both by the length of the vector and by the color, with the colormap indicated to the right. Part (b) shows the velocity field just above the dermal denticle, in this plane vorticity may be found in the rectangle x∈[−0.05,0.1] and y∈[0.1,0.2]. The dermal denticle is cropped to only be overlaid in a region in which flow was not observed. Another signature of vortex formation appears in the lower left corner, rectangle with x∈[−0.3,−0.1] and y∈[−0.22,−0.15]. As in part (a), the local flow speed is indicated both by the length of the vector and by the color. Part (c) shows the flow well above the dermal denticle, now very uniform in the overall flow direction. The local flow speed is indicated both by the length of the vector and by the color. Part (d) shows a map of the rotation field, for the velocity field also shown in part (b). The color map indicates the rotation in units of 1/s, spanning the range [−450 s−1, 450 s−1].
Figure 5
Figure 5
Average vector field of the flow near denticles from the Greenland shark, sample from position b12. The image is obtained by patching 48 individual images from fields-of-view obtained with the 10× objective and the PIV processing software. The denticle is “visible” as the white area in the middle with no flow pattern; to guide the eye a black handdrawn line sketches the outline of the denticle. Each of the 48 individual images cover an area of width 580 μm, and height 450 μm. Within each of the 48 individual images, the colormap is similar to that in Figure 4 such that the longest velocity vector is very dark red and the shortest are dark blue. Signatures of recirculation appears in the rectangle with x∈[−5,−4] and y∈[3.4,4.2].
Figure 6
Figure 6
Average vector field of flow near denticles from the Greenland shark, sample from position b12, now seen from above. The image is patched from 21 individual images with fields-of-view obtained with the 10× objective and the PIV processing software. A microscope image of a denticle from the b12 area is scaled and overlaid the patched image of the flow field to roughly show the position of the denticle, in the flow field it was “visible” as a white area in the middle with no flow pattern. Each of these 21 individual images cover an area of width 580 μm, and height 450 μm. The two insets or zooms are examples of such individual images and they illustrate details not visible in the combined image. Within each of the 21 individual images, the colormap is similar to that in Figure 4 such that the longest velocity vector is very dark red and the shortest are dark blue.
Figure 7
Figure 7
Flow pattern in the (x,y) plane, overlaid with z components of the vorticity field. No-slip boundary conditions are assumed at top ((x,y)-plane at z=0.5mm), bottom ((x,y)-plane at z=0mm) and sides ((x,z)-planes at y=0mm and y=4mm), as well as at the surface of the dermal denticles. Part (a) shows the flow field in a height of 100 μm from the bottom surface, part (b) in a height of 200 μm from the bottom surface. The vector field is plotted logarithmically with a range quotient of 1000 between shortest and longest arrow. The small marker below the ordinate axis is at position x=1.6μm in both cases.
Figure 8
Figure 8
Parts (a–c) shows the flow pattern in the (y,z) plane, overlaid with x components of the vorticity field, with the same no-slip boundary conditions as in Figure 7. Panel (a) shows the flow in a reference position, and panels (b), and (c) are translated along x by 100 μm and 200 μm, respectively. Part (d) shows the flow pattern in the (x,z) plane, at the symmetry plane of the denticle, overlaid with y components of the vorticity field, with the same no-slip boundary conditions as in Figure 7. The vector field is plotted logarithmically with a range quotient of 1000 between shortest and longest arrow.
Figure 9
Figure 9
(Color online) Setup, with details. Part (a) shows an overview of the elements of the μ-PIV system, consisting of Flowmaster Mitas with a pulsed laser, a sensitive camera, and computer with μ-PIV software. Drawing courtesy of Gitte Frederiksen. Part (b) shows a sketch of the combination of fluidics and μ-PIV instrument, with part (c) and (d) providing details of the microfluidic chambers. The shark skin samples are mounted in the right (c) or upper (d) rectangular part of the chamber (blue online) with the liquid flowing in the left (c) or lower (d) slightly larger rectangular part of the chamber (red online). The base (yellow online) illustrates the additional void in the PDMS part that allows for cutting the PDMS before attaching it to a microscope glass slide, then serving as base for the entire chamber and ensuring the closure of the liquid chamber.
Figure 10
Figure 10
Top: Overview of the modelled geometry in COMSOL. Lower: The CAD model for a single denticle.
See this image and copyright information in PMC

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