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Sophisticated Energy Shield Found in a Shrimp

Photo credit: Cédric Péneau, CC BY-SA 4.0 , via Wikimedia Commons.

How many showstoppers does it take to stop a show? And how many unique irreducibly complex mechanisms does one organism have to exhibit to falsify Darwinism? “One” should do in answer to both questions. The mantis shrimp has several, enough to make the rubble bounce on an evolutionary fitness landscape.

The mantis shrimp (Odontodactylus scyllarus) has attracted the attention of scientists for years now, particularly those interested in biomimetics. This brightly colored and googly-eyed creature, looking like a monster from an alien planet, has found solutions that engineers would like to imitate. Its strange-looking, cross-hatched rainbow eyes, for instance, are constantly moving without making the animal dizzy, and it is the only animal known to distinguish circularly polarized light. Its larvae come with flashlights on their eyes. And it has one of the fastest hammers in the living world: a “dactyl club” strong enough to shatter the hard shells of its prey. 

How to Pack a Punch

Tropical fish hobbyists know to avoid putting these creatures in their aquariums, because the mantis shrimp’s hammer-like blows can break glass. Emily Reeves wrote about investigations by Stuart Burgess about this hammer that employs a four-bar linkage mechanism. “When the shrimp is ready to punch, it relaxes a muscle, the latch is released, and the accumulated elastic energy delivers 1000 N of force.” A new measurement described below puts that at “~1500 N (i.e., exceeding 1000 times its body weight).”

Therein lies a puzzle: how does the mantis shrimp avoid injuring itself? One would think that a biological tool capable of smashing glass and hard shells would get one shot before being sent back to the repair shop. Yet the mantis shrimp can deliver blow after blow between molts without cracking its proteinaceous hammer. 

How Does It Do It?

Scientists suspected that the club must contain special energy-absorbing properties. They could observe layers of proteins and minerals on the club’s tissue, but measuring the forces on such a small object during its rapid action has been difficult. Now, a team of mechanical engineers at Northwestern University, led by N. A. Alderete and H. D. Espinoza, has succeeded in measuring the impacts at the nanoscopic level. They determined that the precise arrangement of proteins in those layers create a “phononic shield” that absorbs and distributes the energy. Their results were published in Science. Mark S. Lavine summarized the results this way:

The mantis shrimp is known for its ability to rapidly and forcefully strike its prey, both directly and due to the rapid collapse of cavitation bubbles, without sustaining significant damage. Much of this ability has been attributed to the complex multiscale organization of the structure of the shrimp’s dactyl club and its resultant mechanical properties. Alderete et al. used fast spectroscopy techniques to disclose the effect of the club structure in terms of its phononic shielding abilities… showing that it can effectively filter shear waves to mitigate impact forces during strikes. [Emphasis added.]

Shear waves are known to be destructive; they can cause traumatic brain injuries and nerve damage in humans. As waves, though, they can be compared to sound waves and light waves. They traverse space with particular wavelengths and frequencies that can be reflected, refracted, intensified, or attenuated. Since a phonon of sound energy corresponds to a photon of light energy, the authors draw a parallel between a “phononic shield” and the photonic crystals that intensify or cancel colors in butterfly wings and bird feathers:

It has been proposed that the Bouligand structure [more on that below] also endows the dactyl club with shear wave–filtering capabilities in the form of ultrasonic phononic bandgaps (i.e., select frequency ranges at which the propagation of elastic energy is forbidden or strongly attenuated). Although phononic bandgaps have been put forward as an optimized engineering strategy for prey-predator interactions, experimental evidence of phononic behavior in nature remains rare, particularly when compared with the more extensively documented biophotonic phenomena. Notably, experiments have shown that the scales covering the wings of certain moth species have evolved to absorb sound waves, through local resonance in the 20- to 160-kHz range, and provide acoustic camouflage against the echolocating sonar of predatory bats.

Engineers have profited from imitating the photonic crystals found in nature. The brilliant blue color in the wing of a Morpho butterfly, for instance, results from microscopic patterns on the scales that intensify the blues and cancel out other wavelengths. Biomimetics engineers are learning to design surfaces with “structural color” instead of pigments by imitating the microscopic geometry of photonic crystals in nature.

What Is This Bouligand Structure?

The “Bouligand structure” of proteins in the mantis shrimp’s dactyl club has a similar effect on shear waves resulting from the mantis shrimp’s powerful blows. By definition, it is a material consisting of stacked layers that are rotated with respect to one another to provide strength, as in plywood. The figure in the paper shows layers of mineralized chitin fibers standing upright, forming walls perpendicular to the wave’s energy. These walls vary in density and angle but are not rotated at random; the pattern repeats every 500 micrometers or so.

A football analogy may help. We’ve seen the upright pillars of rubber-coated foam dummies that players use to practice their runs and tackles. Picture row after row of practice dummies, lined up like ranks of soldiers, that a football team needs to charge through. These practice dummies, though, are not arranged with geometric regularity. One row may be upright. The row behind it might be tilted at an angle. The next row is tilted at a steeper angle. Behind that, a row may be stacked vertically. This quasi-random arrangement is repeated dozens of times. Now, picture the football team trying to charge through this maze toward the touchdown goal. An individual linebacker may have no trouble knocking over one dummy, but he is going to get lost and confused by the pattern. It will distract him leftward one moment and rightward the next, until he has lost all sense of direction and is transferring all his energy to the dummies and not to the planned direction of motion. The team’s progress is stunted by the arrangement of the pillars in its way. No energy is lost due to the First Law of Thermodynamics, but the players dissipate their energy in the structure and never make it through.

The Bouligand structure of the mantis shrimp’s dactyl club is even more effective, because its energy absorbing properties are wavelength dependent. Shear waves of shorter wavelength may get absorbed like the hapless football players, but longer wavelengths can make it through the obstacle course just fine. This is analogous to how the James Webb Space Telescope, tuned to infrared wavelengths, can see through dust clouds that are opaque to the Hubble Space Telescope. For the mantis shrimp, its lethal energy gets directed through the club to the prey, but the shear waves that would damage the club are scattered and attenuated. The club survives undamaged to deliver another hammer blow. All this occurs in “a well-orchestrated strike sequence that spans over seven orders of magnitude in time (from hundreds of milliseconds to nanoseconds),” the authors say. Half the energy comes from the initial strike; the other half comes from the collapse of cavitation bubbles “with frequency contents that can reach hundreds of MHz.” Scientists lacked the instrumentation to detect these energies till now.

A Bandgap Filter

The authors call the protective layers a bandgap filter. The term is familiar to acoustic engineers. Software makes it easy these days to filter out unwanted frequences in a soundscape. I’ve used software tools like this myself, like when trying to filter out wind noise in a nature video. The sound engineer can roll off low frequencies or high frequencies or drop out particular frequencies like the 60 Hz hum of a fluorescent light. If I had to design a physical structure to filter out a specific frequency range but permit others, I would be at a loss! The mantis shrimp comes supplied with a bandgap filter made of protein that works very effectively. How did that come about? Did the shrimp dream up this strategy on its own?

A remarkable aspect of the paper is the authors’ use of design language. Sure, they claim that this wonderful bandgap filter “evolved” like the phononic shield in the moth’s wing. But those claims lose their force against praise language for the elegance of the structures they observed.

The mantis shrimp’s design, which selectively shields against the highest frequencies rather than the entire spectrum, reflects an advanced strategy that recognizes that strain rate can be as damaging as, or more damaging than, load magnitude, a phenomenon observed in studies on the effects of ultrasound. This selective filtering also relates to the overall size limitation of the periodic region within the dactyl club, given that filtering lower frequencies would require larger pitches. Furthermore, the periodic region provides additional advantages, including enhanced toughness attributed to the Bouligand architecture. This architectural motif offers dual benefits: high-frequency phononic filtering and mechanical toughening. Interestingly, these phenomena may not be independent but rather interdependent, with phononic mechanisms potentially enhancing extrinsic toughening by facilitating stable crack growth and mitigating catastrophic failure.

“A Paragon of Biological Engineering”

In their conclusion, the authors state that the mantis shrimp has “long been regarded as a paragon of biological engineering” due to its “notable impact-related properties.” They note “the hierarchical structure” of the mineralized proteins in the filter is responsible for its ability to mitigate impacts.1

The word “hierarchical” brings to mind “irreducibly complex.” A beneficial mutation would have no foresight to work toward the creation of a hierarchical structure exhibiting a strategic function. How many shrimp had to bust their arms on hard shells before enough lucky mutations arrived for this to work? A starving shrimp would not leave offspring, but if it had other food sources, it would not need the dactyl club.

This bandgap filter looks designed and works like a designed mechanism. Commenting on this paper in the same issue of Science, Pablo D. Zavatierri uses the word design, too. He thinks there may be more examples to discover.

The interplay between structural hierarchy and wave properties also prompts consideration of whether phononic bandgaps exist in similar structural motifs of different species. For example, the helicoidal structures in beetle wings have good strength and are fracture resistant. The discovery of other natural phononic structuresand understanding their limitations could unlock new designs with capabilities beyond existing impact-resistance materials and energy dissipation systems.

Davide Castelvecchi at Nature also took note of the design implications of the discovery, saying that the findings “could be used to make surgical implants that can harvest energy beamed through tissue in the form of ultrasounds, or mechanical filters for mobile phones and other electronics.” Could jackhammers and guns without recoil be on the horizon?

In an Arthropod? Wow!

For the first time, the authors say, scientists have found a structure able to “extend the known range of functional phononic behavior into the MHz regime… as a biological functionality.” They dream of applications for this strategy:

Additionally, this work highlights nature’s ability to engineer a high-quality ultrasonic chirped phononic crystal, exhibiting Bloch harmonics, with a level of sophistication that would typically require advanced micro- and nanomanufacturing techniques. Furthermore, the discovery of flat bands extending into the hundreds of MHz suggests the potential for spatial energy localization, which can be dissipated locally with minimal damping, offering further insights into how these natural structures may mitigate high-frequency energy.

A high-quality, functional, hierarchical bandgap structure “with a level of sophistication that would typically require advanced micro- and nanomanufacturing techniques” — in an arthropod? I think that statement deserves a “Wow” icon beside it. As stated above, it only takes one showstopper to stop a show. The Evolution Theater will have to close up shop when enough young bioengineers rally to the long-running Intelligent Design series across town.

Notes

  1. “A major contributing element to the dactyl club’s strike power is its hierarchical design, made from a limited but exquisitely tuned arrangement of mineral and organic materials. Three distinct layers make up the club from the exterior to the interior: the impact surface, the impact region, and the periodic region (Fig. 1C). The impact surface is a hard (~60 GPa), thin (~70 μm) hydroxyapatite coating that prevents catastrophic failure by exhibiting viscoplasticity and localized damage. Next, the impact region (~500 μm) consists of mineralized chitin fibers in a herringbone architecture, which enable damage dissipation through diffuse cracking, crack arrest, and crack deflection. Last, the periodic region features a spatially graded Bouligand arrangement of chitin fiber bundles [~80- to 10-μm pitch (p), 2° to 6° interlayer rotation angle (ψ)], which modulates stress wave propagation during impact, akin to a backing layer. Together, these region-specific mechanisms form a synergistic protection system that withstands repeated high-intensity impacts without substantial damage.”