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This reprint is provided for personal and noncommercial use. For any other use, please send a request to Permissions, American Scientist, P.O. Box 13975, Research Triangle Park, NC, 27709, U.S.A., or by electronic mail to [email protected]. ©Sigma Xi, The Scientific Research Society and other rightsholders FEATURE ARTICLE

The Most Powerful Movements in Biology

From jellyfish stingers to shrimp , it takes more than muscle to move extremely fast.

S. N. Patek

began to observe colorful pea- duous search to access a high-speed and evolutionary trade-offs accom- cock , predatory imaging system capable of showing panying extreme movement, and the that smash snails me something more than just a blurred technical applications of biological dis- with a hammer-shaped append- motion, I finally filmed strikes in slow coveries. Iage, when I was a postdoctoral fel- motion. The images were so extraor- low in Roy Caldwell’s laboratory at dinary that I knew on that first day It’s All About Power the University of California, Berkeley. of data collection that we had stum- Once we began analyzing those first The mantis shrimp’s process of break- bled upon something remarkable. The high-speed images of smashing mantis ing a snail was a delight to observe. movements happened within only a shrimp, the movements were far fast- They probed, wiggled, and positioned few frames even when filming at 5,000 er than anyone could have imagined. a snail into place. Just before smash- frames per second—suggesting ex- Their hammer-shaped mouthparts, ing the snail, they touched the snail’s treme speeds and accelerations. A bril- called raptorial appendages, accelerate surface with antennules, possibly to liant bubble was visible between the like a bullet in a gun (100,000 meters per attain a sense of the position and sur- hammer and the shell. Indeed, I soon second squared) and achieve speeds up face of the target. After what anthropo- realized that, contrary to my expecta- to 31 meters per second that rival high- morphically felt like an inhale before tions, the fastest biological motions are way traffic moving at 69 miles per hour. a dive, the mantis shrimp struck. The not generated by cheetahs, the blink The duration is so brief that more than strike itself was invisible—too fast to of an eye, or an escaping fish; instead, 100 of these strikes could fit within one see with the naked eye—but a loud they occur in small, obscure creatures blink of an eye. A human needs to use a pop occurred, and new shell fragments that have harnessed one of the great robust hammer-blow to break the same appeared on the substrate. Then, the challenges in physics and engineering: snails that these small crustaceans can cycle began again: probing, wiggling, extreme power output. fracture with raptorial appendages that positioning, touching, “inhaling,” and Over the subsequent years that I are smaller than a child’s pinky finger. then, “pop,” another invisible but loud worked on extremely fast systems, this movement inevitably in- strike occurred. Silence reigned in the emerging field has yielded results that vokes the role of muscle, but it turns tank when the mantis shrimp finally surprise and unsettle the standard ex- out that to achieve these extraordinari- began to eat the tasty morsel once pro- pectations for what is “fast” in biology, ly powerful movements, organisms tected by its shell. During these first while also offering treasure troves of must actually find ways to circumvent observations, it never occurred to me information at the interface of biology, muscle’s limitations. A simple analo­ that I was witnessing one of the fastest physics, and engineering. The realm of gy explains the conundrum. Imagine biological movements on the planet. ultrafast life is populated by extraor- throwing an arrow at a target, just I wanted to see and measure these dinarily fast creatures, such as jaw- using your arm muscles. The arrow “invisible” movements. After an ar- jumping trap-jaw , self-launched would not go particularly far or fast. fungal spores, ballistic jaws, However, if you use those same arm and stinging jellyfish. They challenge muscles to flex a bow and then release S. N. Patek is currently a Guggenheim Fel- our assumptions about why organisms the arrow with your fingers, suddenly low and an associate professor in the biology move fast and the costs that accom- the arrow easily reaches and punctures department at Duke University. Patek received pany such extreme capabilities. Mantis its target. The energy input is the same a bachelor’s degree from Harvard University and a PhD from Duke University. Patek’s shrimp have received the most inten- whether or not a bow is used. The only research focuses on the interface between phys- sive examination of any system in this difference is the time over which the ics and , primarily in the realm of realm and are now a key system for energy is released. With just an arm ultrafast systems and invertebrate acoustics. probing the deep evolutionary history muscle, the energy output occurs over E-mail: [email protected]. of extreme weaponry, the mechanical a relatively long time period. With the

330To see American more about Scientist, mantis Volume shrimp 103and trap-jaw ants go to bit.ly/1GoBWbq. Mantis shrimp, such as this one using its hammer-like to smash a snail shell, pro- The result is … no movement at all! duce some of the fastest movements of any organism. Understanding these movements sheds The system is primed to strike as soon light on their evolution and generates new knowledge for engineering solutions. (Photograph as the flexor muscles relax, release the courtesy of Roy Caldwell.) latches, and permit the stored elastic energy to release over an extremely addition of a bow, the energy release rial appendages use extensor muscles short time period to push the hammer occurs over extremely short time scales. to swing out their hammer and flexor forward with extreme power output. The result is power amplification—the muscles to fold appendage segments To varying degrees, this is the trick crux of all ultrafast movements. Power toward the body during normal, daily that all high-power systems use: They is defined as work divided by time. By activities. However, when they need to temporally and spatially separate slow decreasing the time over which work is do a high-powered blow, they contract loading and energy storage from the performed, power is amplified. the flexor and extensor muscles simul- rapid release of energy that confers Just like the bow and arrow exam- taneously (similar to the antagonistic power amplification. Trap-jaw ants re- ple, mantis shrimp raptorial append- leg muscle contractions that we do pri- lease tiny latches that block their pre- ages contain a spring and a latch to or to a jump). When they co-contract loaded mandibles. Two droplets slowly generate extreme power amplification. these muscles, the large, bulky exten- grow until the point at which they fuse Their mechanism for power amplifi- sor muscles compress an elastic system over exceedingly short time scales to cation is just a tweak to the standard and tiny flexor muscles pull latch-like yield the power to launch a fungal bal- antagonistic muscle contractions mineralizations of their apodemes listospore. The jellyfish’s stinger waits that characterize most ’ mo- (tendons) over a small lump inside the within a slowly pressurizing cell; a trig- tor systems. Just like the extensor and appendage, thus providing effective ger hair dramatically releases the stored flexor muscle pairs that extend and mechanical advantage over the high pressure and ejects the stinger toward flex our limbs, mantis shrimp rapto- forces of the large extensor muscles. its target. Thus, whether a muscle-based www.americanscientist.org © 2015 Sigma Xi, The Scientific Research Society. Reproduction 2015 September–October 331 with permission only. Contact [email protected]. G. espinosus G. platysoma G. annularis G. affinis G. childi G. smithii G. chiragra N. oerstedii 6 N. bredini N. bahiahondensis G. falcatus smashers G. graphurus T. spinosocarinatus C. hystrix Gonodactyloidea C. excavata C. tweediei H. glyptocercus H. trispinosa E. guerinii P. folini O. havanensis O. scyllarus O. cultrifer O. latirostris A. pacifica K. mikado B. plantei A. orientalis 5 S. empusa Squilloidea 7 S. rugosa spearers H. harpax F. fallax P. marmorata Parasquilloidea L. sulcata L. maculata A. vicina A. tsangi Lysiosquilloidea 3 P. ihomassini H. tricarinata C. scolopendra R. hieroglyphica R. ornata R. pygmaea 2 R. komaii Pseudosquilloidea R. oxyrhyncha 4 P. richeri 1 P. ciliata H. californiensis Hemisquilloidea H. australiensis P. longipes A. tasmaniae N. americana outgroup H. americanus intermediates M. norvegica

300 250 200 150 100 50 0

million years ago

This abridged version of the family tree of more than 450 mantis shrimp shows that ments in water. One region of water smashers evolved from spearer-like ancestors. Ancient mantis shrimp also had rapto- moving extremely quickly relative to rial appendages. Understanding the diversity and evolution of mantis shrimp appendages adjacent regions yields low pressure lends insight into the costs and benefits to moving ultrafast. (Figure adapted from T. Claverie that can form vapor bubbles. A para- and S. N. Patek, 2013.) gon of power amplification, cavitation bubbles collapse over such short time movement or a fluid-driven motion, the mation and collapse of a large bubble periods that a massive, transient re- underlying mechanisms of ultrafast sys- between the mantis shrimp’s hammer lease of energy occurs in the form of tems are all about power amplification. and its prey. I immediately recognized intense heat (similar to the surface of the Sun), light, and sound. Engineers have had their own travails due to cav- itation in fast-moving systems: Rapid- We had expected that the animals with ly rotating boat propellers self-destruct due to cavitation bubble collapse, and the fastest weapons would be targeting fast-moving submarines generate loud noise from cavitation bubbles collaps- the fastest prey. ing, which inevitably detracts from stealthy missions. While cavitation-based weapon- ry was already known to biologists Wielding Weapons in Water this bubble as a primary source of the through the curious cavitation bubble The other remarkable feature of those popping noises in the lab: It was cavi- projectiles of snapping shrimp (distant first high-speed images of mantis tation, a fluid dynamic process that relatives of mantis shrimp), the forces shrimp strikes was the dramatic for- happens during extremely fast move- of cavitation had yet to be measured in

332 American Scientist, Volume 103 © 2015 Sigma Xi, The Scientific Research Society. Reproduction with permission only. Contact [email protected]. these biological contexts. Intrigued as to whether cavitation bubble collapse generates measurable forces during mantis shrimp strikes, I developed an approach using piezoelectric sensors sampled at extremely high rates that ultimately detected the forces pro- duced by both the impact of the ap- pendage and those generated by the collapse of the cavitation bubble. This discovery yielded the first insights into the roles of impact and cavitation for high-speed prey capture in biology. In particular, we discovered that each ultrafast hammer blow by a mantis shrimp essentially strikes twice—once with the actual physical impact of the hammer and the second with the po- tent pressure waves of cavitation bub- ble collapse. Yielding rotational movements that rival the best-performing mantis shrimp, Suzanne Cox (a former gradu- ate student in my laboratory, now at the University of Massachusetts Am- herst) built Ninjabot, a physical model of mantis shrimp, to test the thresholds and conditions for cavitation and im- pacts during rapid rotation—a central Spearing mantis shrimp, such as the Lysiosquillina sulcata pictured above, are predators that issue for cavitation-resistant boat pro- stab quick-moving fish. Although their prey are faster than snails, they move their append- peller design and ultrafast impacting ages at a fraction of the speed and acceleration of their snail-smashing relative. This observa- systems. Ninjabot allows us to swap tion indicates that there is a trade-off between spring-loading quickly and packing a powerful out real appendages with a variety of punch. (Photograph courtesy of Roy Caldwell.) model shapes and materials to system- atically test questions about fracture hammer that enables this impressive carbonate. Within the hammer, the ma- mechanics, materials, and cavitation. performance. They discovered that the terials are layered to dissipate energy One intriguing finding is that man- outermost layer of the hammer is very and concentrate microcracks within the tis shrimp appendages don’t cavitate hard and highly mineralized, primarily hammer rather than at its surface. during ultrafast rotation, but when the composed of concentrated phosphorus These discoveries of the structural appendages are attached to Ninjabot, (for instance, calcium phosphate) and principles of impact fracture mitiga- they do cavitate. Thus, even holding the typical material, calcium tion in mantis shrimp appendages the kinematics, materials, and shapes constant between a live mantis shrimp and Ninjabot, another factor seems to eyes be suppressing rotational cavitation in mantis shrimp. The answer to this un- antennules resolved discovery may hold hints for carapace abdomen designing propellers to reduce cavita- tion damage. raptorial telson A mantis shrimp’s rapid-fire, high- appendage impact, and cavitation-based assaults on snail shells occur with a substantial risk of damaging the mantis shrimp’s own appendage. Indeed, snail shells have been heralded as one of the most unbreakable materials in biology—yet dactyl gills mantis shrimp manage to crack them dactyl (hammer) without fracturing their own append- ages. Intrigued by this unusual ability, a research team led by David Kisailus at the University of California, River- Mantis shrimp are crustaceans with specialized raptorial appendages for capturing prey. This side, revealed the material composi- peacock mantis shrimp ( scyllarus) has a hammer-like appendage for smash- tion and structural arrangement of the ing snail shells. (Photograph courtesy of Roy Caldwell.) www.americanscientist.org © 2015 Sigma Xi, The Scientific Research Society. Reproduction 2015 September–October 333 with permission only. Contact [email protected]. have already inspired new impact- doors to more broadly considering the One obvious explanation for the small resistant materials. Again from the Ki- principles of ultrafast rotation in wa- number of ultrafast creatures is that sailus group, researchers used small ter, cavitation dynamics, and impact- we have yet to discover all of them chunks of carbon fiber–epoxy mate- resistant materials. Whether in engi- presently inhabiting our planet, given rials and shaped them into a helicoi- neered or biological systems, such as that these movements are invisible to dal arrangement similar to the mantis the impact-resistant materials of trap- the naked eye. Before filming mantis shrimp with extreme high-speed im- aging, we certainly had no concept of their real capabilities. That initial It takes a lot of time to be ultrafast. and unexpected discovery in mantis shrimp has inspired our continued examination across many branches of the tree of life for as-yet undiscov- shrimp’s hammer architecture. They jaw mandibles, microscopic punc- ered ultrafast creatures—leading to then tested the impact and fatigue re- turing spears in jellyfish, or cavitation subsequent research on trap-jaw ants sistance of the new material compared bubble-wielding snapping shrimp, that jump with their ultrafast jaws as to the mantis shrimp’s hammer at sim- these early discoveries pave the way well as the near-invisible launching of ilar size scales. Ultimately, the materi- to more fully understanding the multi- fungal ballistospores. It is also likely, als inspired by mantis shrimp may be disciplinary implications of the realm however, that a network of trade-offs used in lightweight, high-speed im- of the ultrafast. guides and limits biological diversifi- pact systems for humans. cation, and that ultrafast systems come The challenges of wielding high- No Such Thing as a Free Lunch with some substantial limitations. impact weapons are not unique to It seems like any organism would Our first hint of broad underly- mantis shrimp. Each of these discover- benefit from extreme kinematic capa- ing limitations on ultrafast systems ies made through intensive analysis bilities, but only a handful of ultrafast came when we decided to film a dif- in this one model system has opened organisms have been documented. ferent type of mantis shrimp than the hammering variety we initially stud- ied. The evolutionary tree of mantis duration speed acceleration shrimp reveals that snail-smashing is (orders of magnitude) the anomaly and that the large majori-

7 ty of mantis shrimp are spearers, which 0.7 microseconds 67 meters per 10 meters per spear or stab evasive prey with elon- nematocysts second second squared gated, spiny raptorial appendages that trap-jaw ant jaws nematocysts 10 microseconds termite jaws lack a hammer. Based on molecular fungal spores 106 meters per and analyses, smashers evolved 58 meters per second squared from spearing mantis shrimp about 50 second 25 microseconds trap-jaw ant jaws million years ago. After measuring the termite jaws gyrfalcon dive 105 meters per fascinating speeds of smashing mantis 37 meters per shrimp, my former graduate student 100–300 second second squared microseconds nematocysts smashing mantis Maya deVries (now at Scripps Institute trap-jaw ant jaws shrimp of Oceanography) and I thought that bladderwort trapdoor 31 meters per fungal spores we would find even more impressive second kinematics in the spearers. That turned smashing mantis shrimp 103 meters per 1–6 milliseconds out not to be the case. In fact, spearers mantis shrimp strike 25–26 meters per second squared spearing mantis move at a small fraction of the speeds second and accelerations of smashers. 10 milliseconds cheetah sprint shrimp grasshopper jump snapping shrimp water jet bladderwort uid ow The finding that fish-catching spear- ers move far more slowly than smash- 102 meters per 0.1 seconds 2–3 meters per ers was counterintuitive; we had ex- second second squared jump pected that animals with the fastest fungal spore escaping sh weapons would be targeting the fast- 0.3 seconds frog jump squid strike blink of an eye grasshopper jump grasshopper jump est prey. In fact, as we looked deeper bladderwort uid ow into the habits of ultrafast creatures, 10 meters per ~10 meters per we found that most do not target fast second squared prey. Instead, the very fastest animals second cheetah sprint target defended, hard-shelled prey fastest human runner frog jump that typically do not quickly evade attack. If the biological machinery is present that could rapidly nab jump- Ultrafast organisms, such as mantis shrimp and trap-jaw ants, move much faster than the ing or swimming prey, why wouldn’t blink of an eye or a sprinting cheetah. Jellyfish stinging cells, called nematocysts, also top the ultrafast animals hunt evasive prey? charts of the ultrafast. As high-speed imaging technology has improved, what fast means is One central trade-off of ultrafast being redefined. systems—including mantis shrimp,

334 American Scientist, Volume 103 © 2015 Sigma Xi, The Scientific Research Society. Reproduction with permission only. Contact [email protected]. trap-jaw ants, jellyfish stingers, and bow and arrow human engineered systems—revolves­ around the loss of control of the weapon once it is released. For ex- ample, when using a bow and arrow to hunt prey, the arrow is preloaded and aimed, but once the arrow is re- leased, the archer cannot adjust its course and the arrow will only strike its target if the prey remained station- latch latch ary. Ultrafast animals are so fast that underlying neurons cannot monitor or modify the movement once it has be- gun. Whether a trap-jaw ant, smashing termite, or a mantis shrimp, once they have released their ultrafast weapon- ry their neurons cannot send signals fast enough to relay and modify the system in real time. In an analysis of muscle activity prior to ultrafast move- ment, a former postdoctoral fellow in my lab (Katsushi Kagaya, now at mantis shrimp raptorial appendage the Seto Marine Laboratory in Japan) demonstrated that mantis shrimp vary strike velocity through modifica- extensor saddle extensor saddle tions to muscle activity during spring muscle muscle loading, but once the strike begins the movement is too fast to permit adjust- ments by the nervous system. Another biology-specific trade-off tendon for ultrafast systems is almost a brain- teaser: It takes a lot of time to be ul- latch tendon latch trafast. Coming back to the principle exor exor of extreme power amplification, the muscle muscle key features are stored potential en- ergy (typically in springs) and rapid energy release (through a latch). This means that energy is stored in advance Ultrafast movements like that of the smashing mantis shrimp’s appendage work as a spring-loaded­ and released extremely quickly. For system, much like a bow and arrow. In these systems, a spring-like mechanism stores potential ultrafast systems that use muscle, this energy, which is rapidly released by a latch-like mechanism (in this case, the flexor’s tendon). trade-off is especially apparent. Mus- cles cannot contract both forcefully in ultrafast systems. We found that re- enough to capture evasive prey, thus, and quickly. The fundamental build- gardless of whether they are spearers counterintuitively, the predators of ing block of muscle—the sarcomere—­ or smashers, mantis shrimp have rela- evasive prey can respond more quick- contains the myosin and tively long sarcomeres in the muscle ly, but move at slower speeds. Simply actin that bind together to generate that loads the spring, meaning that put, it takes longer to be faster, and the canonical striated muscle contrac- they have force-modified muscles any muscle-based ultrafast system will tion. With longer sarcomeres, more ac- that are good for loading stiff springs. encounter this trade-off during evolu- tin–myosin bonds can be formed at a However, the spearing mantis shrimp tionary diversification and thus poten- given instant, and the overall force of that target evasive prey have shorter tially limit the broader use of ultrafast the muscle increases. However, if more sarcomeres than smashers, by up to systems in biology. bonds are formed at a given instant, 50 percent. Although the behavioral Reflecting these significant trade- then the rate of bond formation and data have yet to be collected, the mor- offs in ultrafast systems, our large- release decreases, resulting in a slower phological data suggest that smashers scale evolutionary analyses of mantis muscle contraction. In sum, longer sar- evolved longer sarcomeres to com- shrimp morphology again revealed comeres permit more force by a mus- press more forceful springs and thus that achieving extreme kinemat- cle but at a slower contraction rate. wield a potent strike, but at the cost of ics comes at a cost. In collaboration Making use of the evolutionary the rate of loading the system. In other with a former postdoctoral researcher diversity of mantis shrimp raptorial words, smashers take a long time to in my lab, Thomas Claverie (now at appendages, a former undergraduate load their weaponry, whereas spear- University of Montepellier),­ we found in my lab (Marco Mendoza Blanco) ers are faster at the draw. Ultimately, that the rate of morphological change and I showed how the universal force- this may mean that the fastest animals in smashing raptorial appendages is velocity trade-off in muscle plays out cannot load their weaponry quickly slower than in other mantis shrimp. www.americanscientist.org © 2015 Sigma Xi, The Scientific Research Society. Reproduction 2015 September–October 335 with permission only. Contact [email protected]. cavitation bubbles

collapsing vapor bubble imploding shock wave heat building light emitted

The movement of the smashing mantis shrimp’s appendage (top panel) causes the water around it to move so quickly that low pressure creates vapor bubbles that then col- lapse, emitting energy in the form of light and heat. This process is called cavitation (above), and it poses an engineering problem for fast-moving boat propellers and turbines, damaging materials (left). This process means the mantis shrimp hammer essentially packs two punches: one from the physical strike and the next from the pressure waves of cavi- tation bubble collapse. (Top panel sequence from S. N. Patek and R. L. Caldwell, 2005.) Wikimedia Commons

Associated with this decreased rate Again, our model system of mantis about the reduction of conflict in - are more tightly coordinated changes shrimp offers some lessons. Mantis mals with ultrafast weapons beyond among the mechanical components in shrimp are essentially soft-bodied these studies of mantis shrimp. Per- smashing mantis shrimp compared to creatures, other than their raptorial haps further studies of the ultrafast spearers. The physical demands of a appendages and their telson (armored dynamics of lethal weapons in these tightly integrated ultrafast mechanism tailplate), such that a well-aimed blow and other animals will reveal novel in smashers may well have reduced is very likely to be lethal. However, behavioral and mechanistic pathways the inherent variability of the compo- smashing mantis shrimp resolve their to de-escalating human conflicts. nents, thereby reducing the potential conflicts through a ritualized behavior for evolutionary change. Reduction of in which they strike each other’s tel- The Ultrafast Crosses Disciplines the potential for evolutionary diversi- son. A former postdoc in my lab, Jen- Compared to the day when we ob- fication is a hefty cost for an ultrafast nifer Taylor (now at Scripps Institute tained the first views of a mantis biological system and certainly offers of Oceanography), discovered that the shrimp’s strike and started to peel back a counterpoint to the easy, superficial striking hammer and receiving telson the layers of quirky details and broad notion that ultrafast systems are a pin- interact with similar dynamics to an principles of ultrafast organisms, this nacle of design. ash hitting a baseball and that the new realm of biology has developed One last trade-off is perhaps the ulti- energy returned to the hammer scales into an intensely multidisciplinary­ mate one: Ultrafast weapons are often with the size of the receiving animal. field with a particular relevance to hu- lethal, and for populations and species One tantalizing possibility is that man- man systems and engineering design. to survive in the long run, organisms tis shrimp actually assess each other’s As the field moves forward with hope- must develop strategies to avoid or size through the impact dynamics of ful anticipation for new discoveries of reduce their use against conspecifics. this ritualized fight. Little is known ultrafast creatures, the most significant

336 American Scientist, Volume 103 © 2015 Sigma Xi, The Scientific Research Society. Reproduction with permission only. Contact [email protected]. Mantis shrimp movements are so powerful that fighting is dangerous. Males and females Nüchter, T., M. Benoit, U. Engel, S. Özbek, fighting over food or territory will strike each others’ armored tail, or telson, to size each other and T. W. Holstein. 2006. Nanosecond-scale up. These ritualized displays of prowess allow the animals to avoid coming to fatal blows. kinetics of nematocyst discharge. Current (Photographs courtesy of Roy Caldwell.) Biology 16:R316–R318. Patek, S. N. 2014. and evolution. Science 345:1448–1449. data set for connections to engineer- powerful yet small creatures have Patek, S. N., J. E. Baio, B. F. Fisher, and A. V. ing principles is the deep evolutionary opened many unanticipated windows Suarez. 2006. Multifunctionality and me- history of these systems. Evolving for into physics, evolution, engineering, chanical origins: Ballistic jaw propulsion millions of years and leaving behind and . This world of discoveries in trap-jaw ants. Proceedings of the National a fascinating fossil record that directly was revealed through breakthroughs in Academy of Sciences 103:12787–12792. documents diversifying appendages imaging technology that now readily Patek, S. N., and R. L. Caldwell. 2005. Extreme over time, the mantis shrimp offer a permit scientists to examine extremely impact and cavitation forces of a biological hammer: Strike forces of the peacock man- natural experiment in engineered sys- fast movements and extraordinarily tis shrimp (Odontodactylus scyllarus). Journal tems under a wide range of historical high power biological systems. With of Experimental Biology 208:3655–3664. and present-day conditions. The data discoveries of new ultrafast systems Patek, S. N., D. M. Dudek, and M. V. Rosario. set includes stunning variants of weap- on the horizon, combined with deeper 2011. From bouncy legs to poisoned arrows: onry, modifications of spring shape investigations into basic and applied elastic movements in invertebrates. Journal and function, trade-offs in muscle per- science, this remarkable realm of bio- of Experimental Biology 214:1973–1980. formance, and habitats including mud, logical capabilities has newly emerged Patek, S. N., W. L. Korff, and R. L. Caldwell. sand, and live from the intertidal as an exciting, multidisciplinary field. 2004. Deadly strike mechanism of a mantis down to ocean depths. shrimp. Nature 428:819–820. This diversity of structures, systems, Bibliography Patek, S. N., B. N. Nowroozi, J. E. Baio, R. L. Caldwell, and A. P. Summers. 2007. Linkage ecology, and time periods offers a ma- Anderson, P. S. L., T. Claverie, and S. N. Patek. mechanics and power amplification of the trix of variables that can be mined for 2014. Levers and linkages: Mechanical mantis shrimp’s strike. Journal of Experimen- combinations of traits that work best trade-offs in a power-amplified system. tal Biology 210:3677–3688. Evolution 68:1919–1933. under particular conditions. Trap-jaw Taylor, J. R. A., and S. N. Patek. 2010. Ritu- ants also exhibit extraordinary evolu- Blanco, M. M., and S. N. Patek. 2014. The evo- alized fighting and biological armor: The tionary diversity; in their case, at least lution of muscle in a power-amplified prey impact mechanics of the mantis shrimp’s capture system. Evolution 68:1399–1414. four independent evolutionary origins telson. Journal of Experimental Biology 213:3496–3504. led to ultrafast mandibles, thus offer- Claverie, T., and S. N. Patek. 2013. Modularity and rates of evolutionary change in a pow- ing a data set of the conditions for and Versluis, M., et al. 2000. How snapping shrimp er-amplified prey capture system. Evolution snap: Through cavitating bubbles. Science consequences of the origins of ultra- 67:3191–3207. 289:2114–2117. fast mechanisms. Fungal ballistospores Cox, S. M., D. Schmidt, Y. Modarres-Sadeghi, are found across a massive number of and S. N. Patek. 2014. A physical model of species with a diversity of shapes and the extreme mantis shrimp strike: Kinemat- habitats that can inform the dynamics ics and cavitation of Ninjabot. Bioinspiration & Biomimetics 9:1–16. of droplet propulsion systems. Simi- For relevant Web links, consult this larly, snapping shrimp and jellyfish deVries, M. S., E. A. K. Murphy, and S. N. ­issue of American Scientist Online: stingers exhibit fantastic diversity of Patek. 2012. Strike mechanics of an ambush predator: The spearing mantis shrimp. Jour- http://www.americanscientist.org/ mechanisms and morphology. nal of Experimental Biology 215:4374–4384. issues/id.116/past.aspx From the behavioral dynamics of rit- Grunenfelder, L. K., et al. 2014. Bio-inspired ualized fighting to the stochastic chal- impact-resistant composites. Acta Biomate- lenges of cavitation avoidance, these rialia 10:3997–4008. www.americanscientist.org © 2015 Sigma Xi, The Scientific Research Society. Reproduction 2015 September–October 337 with permission only. Contact [email protected].