Propulsive Beauty is Skin Deep

Beneath the sandpapery skin of sharks, lurks yet another feat of hydrodynamic engineering. The inner, thickest layer of a shark's skin is a white sheath of fabric composed largely of a very tough, rather springy protein called collagen. Collagen is the major fibrous constituent of skin, tendon, ligament, and bone and is probably the most abundant protein in the Animal Kingdom. It accounts for about 30% of the total body weight of mammals and to cite one of the more spectacular examples it's springiness is responsible for much of the energy recovery in the Achilles tendon of kangaroos, enabling these outback bounders to hop farther than they could powered by muscles alone. Collagen owes its wonderful properties to its structure: triple stranded helical coils that are bound together to form fibrils. These fibrils, in turn, lie in helices around a shark's body. In alternating layers, the collagen fibrils describe right- and left-handed helices. These helices are arranged along the body at various angles to the long axis of the shark (from 90 behind the skull to nearly 0 in the caudal fin). This collagenous corset provides a firm anchor for swimming muscles, acting as a kind of external skeleton. Mechanically, this is a very efficient arrangement, affording very little loss of muscular energy. Having muscles attached directly to the external skeleton is also found in crustaceans, and its efficiency explains why even a tiny crab can give a disproportionately painful pinch. Thus, the network of dermal collagen allows sharks to use their swimming muscles most efficiently.

But wait, there's more. In a fascinating 1978 paper, zoologist S.A. Wainwright and his co-workers described the helical collagen network in the skin of a Lemon Shark (Negaprion brevirostris). They found that the muscle attachments to this collagen corset act as a collective external tendon, promoting more efficient transmission of muscular force to the tail. Further, Wainwright's team discovered that changes in the angle of collagen fibrils during swimming prevent tension loss or skin wrinkling on the concave side of the shark, thereby maintaining the body's internal pressure. Thus, muscular energy invested by a shark toward flexing its body during swimming is transmitted rearward and largely recovered by the 'snap' of this collagen corset especially near the caudal fin, where it can contribute most forcefully toward propulsion. The sheer elegance of this mechanism borders on the sublime! Similar helical arrangements of dermal collagen have also been described in dolphins and squids, enabling these creatures to circumvent the limitations of their respective ancestral designs. Such helical collagen networks have been described in all elasmobranchs examined for this feature to date, including the Great White's close relative, the Shortfin Mako. Although no one (to my knowledge, at least) has yet described this feature in the White Shark, it seems a reasonable bet that this species also makes use of the energy-saving qualities of this collagen corset.

Eight years after Wainwright and his co-workers published their description of the collagen corset in the Lemon Shark, paleontologists Wolf-Ernst Reif and David Weishampel published a paper describing the anatomy and mechanics of the crescent-shaped tail in lamnid sharks. In this paper, Reif and Weishampel confirmed that the skin is the most important attachment site for shark swimming muscles and, among other things, described the tendons that transmit muscular energy from the tail stalk to the tail via the lateral keels. Thus, the keels of lamnid sharks serve as a kind of pulley-system, adding the elastic 'snap' of collagen to the tail-lashing power of the posterior trunk muscles. This may explain why even a small-to-medium-sized Shortfin Mako can break a fisherman's leg with a single tail wallop and how this species can repeatedly leap up to 20 feet (6 metres) out of the water. The White Shark is also known to leap on occasion, especially in pursuit of speedy prey, so this energy-efficient tendon system may give this paramount predator the kind of propulsive edge it needs.

 

ReefQuest Centre for Shark Research
Text and illustrations R. Aidan Martin
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