New research reveals the unusual shape, size and pattern of the dermal denticles that cover basking sharks – thought to be unique to this species. Researchers propose that the shape and arrangement of the skin's scales protects the skin while also allowing for the stretchiness required to open and close their colossal mouths during ram filter feeding.
Dermal denticles are small, pointy tooth-like structures that cover sharks' skin, providing armour, reducing drag for swimming and preventing the attachment of parasites. In most sharks, these denticles are miniscule and arranged in a streamlined pattern for optimal hydrodynamics.
However, recent evidence shows that basking sharks (Cetorhinus maximus) possess a radically different arrangement that aligns with their slow swimming speeds and the extreme head deformations that accompany their filter-feeding lifestyle.
"We only noticed that basking shark denticles where so special when we first investigated the bodies of beached specimens for the purpose of studying their oral filter structures," says Mike Schindler, a PhD student in Mason Dean's laboratory at the City University of Hong Kong.
The skin of other sharks feels firm but smooth when you run a hand over their body from front to back, because the denticles are all aligned towards the tail to reduce drag and enhance swimming performance.
"However, when we touched the basking shark's skin with gloves, they quickly ripped apart - a sign that something was very different about the size and alignment of basking shark denticles," says Mr Schindler.
This divergence from the typical shark skin inspired Mr Schindler and his team to investigate the form and function of these biological anomalies.
The team started by examining large-scale skin patterns across the body using laser scanning, then investigating smaller skin patches under microscopes and scanning them using micro-CT to understand how the denticles were organised in three dimensions. As basking sharks are endangered and specimens extremely rare, the team made use of both physical and virtual museum specimens to maximise the available information.
Since basking sharks are very big, after taking morphometric measurements from denticles, including volume, curvature, length and overall shape characteristics, the team then used large-area laser scans and mechanical tensile tests to better understand how the skin functions on a larger level.
The findings, presented at the Society for Experimental Biology conference, reveal surprising new information about basking shark skin that helps us to better understand their feeding behaviour.
Mr Schindler and his team found that the denticles are massive compared to other shark denticles. "While a microscope is needed to see other shark denticles, basking shark denticles reach a diameter of around half a millimetre and are visible with the naked eye," says Mr Schindler.
They also found a change from the flattened hooklike shape of other shark denticles, towards fang-like shapes, pointed in seemingly random directions. They also found no clear variations in denticle shape along the body, which is unusual for shark denticles.
"What makes the basking shark's denticles particularly unique is their arrangement, since they are clumped together in groups to form what we're calling 'paver blocks', tight clusters of denticles in areas where deformations occur due to body motions," says Mr Schindler. This arrangement, in stark contrast to the smooth skin of most sharks, visually resembles the wrinkled skin of an elephant.
Mr Schindler and the team believe that since these blocks are separated by skin folds without denticles, they may promote the extreme stretching of the skin relevant for the enormous expansion of the mouth during filter feeding.
"Interestingly, the denticles of the 'paver blocks' are arranged like floral whorls, so that the denticle crowns overlap the folds and interdigitate with denticles of neighbouring blocks, covering the folds when the mouth is closed," says Mr Schindler.
These denticles are even very different to those of its closest living relatives, including the sand tiger shark, and other ram filter feeders, such as megamouth sharks.
Using fossil records of extinct species of basking sharks, Mr Schindler and his team have been able to peek at the evolutionary history of these denticles. Since they correlate with the presence of filter structures in these extinct species, it suggests that this bizarre denticle arrangement developed in concert with dietary evolution.
"We suspect that, due to this species' slow swimming speed, denticles were released from a constraint, and the 'skin armour' instead took on a novel role in accommodating the stretching ability of the skin and repelling parasites between the folds," says Mr Schindler.
These findings could hold possible applications for informing bioinspired materials where a balance between structural support and directional flexibility are important, such as sportswear or therapeutic bandages.
This project is funded by the Human Frontier Science Program.
