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American Scientist the Magazine of Sigma Xi, the Scientific Research Society A reprint from American Scientist the magazine of Sigma Xi, The Scientific Research Society 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 mantis shrimp appendages, 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 mantis shrimp, predatory imaging system capable of showing panying extreme movement, and the crustaceans 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 Animal 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 ants, self-launched would not go particularly far or fast. fungal spores, ballistic termite 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 evolution, 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 appendage 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 animals’ 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 species shows that ments in water. One region of water smashers evolved from spearer-like ancestors. Ancient mantis shrimp fossils 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.
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