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Sharks shift their spine into high gear

Nature volume 540, pages 532533 (22 December 2016) | Download Citation

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It emerges that a dogfish shark's spine becomes stiffer as the fish swims faster, enabling the animal to swim efficiently at different speeds. The finding could also provide inspiration for the design of robotic biomaterials.

The languorous undulation of a shark cruising along a reef gives little hint of the fish's potential to unleash a burst of high-speed movement when pursuing prey. Writing in the Journal of Experimental Biology, Porter et al.1 reveal how the structural properties of the non-bony, cartilaginous skeleton of the spiny dogfish shark (Squalus acanthias) allow this fish to shift seamlessly between low-speed cruising and high-speed swimming.

A basic principle of aquatic locomotion is that swift swimming requires a stiff spine2. A stiffer body decreases drag and increases energy efficiency (Fig. 1). By contrast, acceleration requires a flexible spine to allow a fish to uncurl its body in a sudden rush3. It was proposed2 that thick fibres in a shark's skin increase the stiffness of the fish as it swims faster. This hypothesis is attractive, but has resisted experimental verification because of the difficulty of getting sharks to swim fast in a laboratory while attached to high-tech instrumentation.

Figure 1: Shark spine stiffness and swimming efficiency.
Figure 1

a, Water eddies (blue swirls) around a swimming fish creates drag that slows the animal down. Arrows indicate water moving away from the fish's direction of motion and contributing to drag. If a fish has a flexible spine, this creates an inefficient swimming posture for swift movement because it generates high drag. However, flexible spine movement can be useful for allowing rapid acceleration. b, If a fish has a stiffer spine, it encounters less drag and can swim efficiently at high speed. Porter et al.1 studied the properties of the spine of the dogfish shark (Squalus acanthias) at different swimming speeds. The authors found that the fish's spine becomes stiffer as the shark swims faster, thus enabling efficient movement depending on the fish's speed.

Porter et al. investigated shark propulsion from a different direction. Rather than considering the fish's exterior, they went right to the core of the matter: the vertebral column, or spine. In bony animals, the vertebrae of the spine are mineralized, rigid, bony structures that do not change shape appreciably during locomotion. Movement of the spine in bony animals occurs through changes in the shape of the intervertebral disks — elastic, but quite firm structures located between individual vertebrae. These disks consist of an outer ring of fibrous connective tissue encasing a gelatinous core. By contrast, sharks have a mainly cartilaginous skeleton: their vertebrae, as well as their intervertebral disks, are made of cartilage, and the vertebrae are so poorly mineralized that they are potential sites of deformation.

In previous in vivo and in vitro work by researchers from the same laboratory4, sharks had tiny piezo-crystal-based monitors implanted on their vertebrae. These sensors emit and detect ultrasound, allowing inter-crystal distances to be measured with micrometre-scale accuracy. The researchers showed that the vertebrae themselves deformed, not just the intervertebral disks. This earlier work showed that the shark vertebral column could not be simplified as a series of soft connectors between rigid blocks, and instead is a structure that can be variably deformed across its entire length.

“The overall result was a fine-scale understanding of the relationship between spinal deformation and swimming speed.”

To investigate changes to the shark spine during swimming, Porter et al. bent excised vertebral columns in the same wave-like motions that are observed during different swimming speeds. The authors used these in vitro experiments, together with computer modelling, to determine the length changes that occur across a spinal segment (a series of ten vertebrae and nine intervertebral disks) when the dogfish shark swims. They recorded the corresponding spinal deformations that occurred during movements ranging from the lazy tail wag of a cruising shark to the all-out burst that precedes prey capture. The overall result was a fine-scale understanding of the relationship between spinal deformation and swimming speed.

As a shark swims, the energy used to bend the spine is stored, and is then released when the spine straightens, providing energy for forward motion. Porter and colleagues' work demonstrates that, in swimming sharks, deformation of the vertebrae as well as the intervertebral disks contributes to the stored energy. The authors also observed that, as sharks swim faster, their spine gets stiffer. The bending of a stiffer spine increases the stored energy that can be used to drive forward motion, and allows the shark to swim faster with greater efficiency. This is an aquatic equivalent of continuously variable transmission, a type of gear-change system found in some motor scooters that is continuously responsive to a wide range of speeds.

What is the structural basis of the shark's remarkable varying spinal properties? Cartilage is a water-laden, fibre-reinforced material. It is a type of in-between substance, neither an elastic solid such as rubber or metal, nor a stirrable fluid such as coffee. Instead, cartilage belongs to the category of viscoelastic materials — materials that resist deformation differently when they change length at different rates. An example of a viscoelastic material is the toy Silly Putty, which can be drawn hair thin when pulled slowly, but which breaks apart before stretching if it is given a sudden pull.

Intervertebral disks, being made of the gooey composite material cartilage, have the viscoelastic property of becoming stiffer when suddenly strained. This is why they make such poor shock absorbers when someone locks their knees straight to jump off a step. Nevertheless, these structures can undergo gradual compression. Over the course of a day, human intervertebral disks are slowly compressed under the weight they bear, leaving people shorter at night than in the morning5. Porter and colleagues' work shows that, like the human version, fish intervertebral disks display the viscoelastic property of an increase in stiffness when the structure is rapidly strained.

Applications for the discoveries made by Porter et al. might arise in the world of soft and bio-inspired robotics, given that microrobots exist that have been designed using the swimming patterns and anatomy of skates, another type of cartilaginous fish, as an inspiration6. This discovery of continuously variable transmission in sharks might enable robotic designers to construct light, energy-efficient systems for motion that would require few moving parts and have potentially low levels of wear or little need for replacement parts.

Porter and colleagues' findings highlight the difficulty of characterizing dynamic mechanics in composite biological materials, a research area that could revolutionize design by introducing materials whose physical conformation can shift to fit differing roles. In an age of climate change and increasing environmental pollution, inventors are increasingly looking to nature for inspiration when trying to build clean and efficient machines. What better animals to choose than sharks, given that their capacity for movement has been refined over more than 420 million years7,8 of evolution?

Notes

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    et al. Zoology 117, 19–27 (2014).

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    Phil. Trans. R. Soc. Lond. 33, 87–88 (1724).

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    et al. Science 353, 158–162 (2016).

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    J. Fish Biol. 80, 918–951 (2012).

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  1. Matthew A. Kolmann and Adam P. Summers are in the Department of Biology, Friday Harbor Laboratories, University of Washington, Friday Harbor, Washington 98250, USA.

    • Matthew A. Kolmann
    •  & Adam P. Summers

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Correspondence to Matthew A. Kolmann or Adam P. Summers.

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https://doi.org/10.1038/nature21102

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