To watch an ant slowly angle its head toward the ground and then disappear with what seems to be a fleeting snap of its jaws, is to witness one of the fastest recorded biological movements on the planet: a mandible-strike of a trap-jaw ant. The fastest motions are not generated by cheetahs (65 mph), the blink of an eye (0.3 s) or an escaping fish (10 g’s); instead, they occur in small, obscure creatures that have harnessed three challenges in physics and engineering: (i) extreme acceleration (ii) at small length and mass scales, and with (iii) repeatable and efficient use throughout the life of the organism.
Work in the Patek laboratory has established the outer extremes of fast movement, including the fastest-described systems that can be used repeatedly (mantis shrimp, trap-jaw ants, and amphipods), and we have examined the principles and performance of a diverse array of many other small, fast systems. Only a handful of labs around the world have the imaging capability to measure these movements: state-of-the art locomotion labs film at 500-5000 frames per second (fps), whereas our fast systems require imaging from 20,000-300,000 fps. Consequently, small, fast systems exemplify the realm of discovery science. We have relentlessly pursued core physical principles while leveraging fast systems to investigate how physics interfaces with evolutionary diversification. We have succeeded in establishing a conceptual, mathematical, evolutionary and interdisciplinary framework, such that this emerging field is now in the growth phase.
The fastest biological movements were once generally thought to have evolved for predator-prey pursuits, like the cheetah’s spectacular running abilities or the sprints of swimming fish. However, as each new ultrafast system was measured or compiled, we have established that organisms use ultrafast movement for puncture (Anderson, et al., 2016, Interface Focus; deVries et al, 2012, J. Exp. Biol.), fracture (Patek and Caldwell, 2005, J. Exp. Biol.; Patek, et al., 2004, Nature), impact (Patek, et al., 2006, Proc. Nat. Acad. Sci.; Spagna, et al., 2008, J. Exp. Biol.), dispersal (Liu, et al., 2017, J. Roy. Soc. Interface; Pringle, et al., 2005, Mycologia), and even sparring (Green and Patek, 2015, Biology Letters; Green and Patek, 2018, Proc. Royal Society B: Biol. Sci.) – a remarkable array of uses far greater than originally recognized.
Latch-mediated spring actuation (LaMSA)
For decades, the field of fast movements has been defined in terms of what muscles cannot do. Power amplification, a widely-used identifier of these systems, indicates that a movement’s power output is greater than possible by muscle contractions. This catch-all is a helpful categorization, yet has unintentionally “black-boxed” how these movements are actually generated (Longo et al, 2019, JEB). In many extreme systems, energy is stored in a spring, released by a latch, and the movement is solely driven by an elastic mechanism. The muscle’s job is relegated to simply putting energy into elastic structures, directly analogous to an archer’s arm muscles loading a bow (Ilton, et al., 2018, Science; Patek, et al., 2011, J. Exp. Biol.). Even so, it is not obvious how springy materials yield extreme power amplification and ultimately circumvent muscle’s power limits.
Hence, we named this class of systems latch-mediated spring actuation (LaMSA) to capture the crucial interplay of springs and latches in these ultrafast systems. (Longo et al, 2019, JEB). Our realization of the “black box” of power amplification came about through a paradox: it takes a long time to be extremely fast. Muscle – and any system, for that matter – faces a tradeoff between velocity and force, such that systems moving at higher velocities generate less force (e.g., hitting a baseball or golf ball) and systems requiring large forces move more slowly (e.g., throwing a shot put, weight lifting). When animals evolve ultrafast movement, they evolve slowly-contracting muscles that produce a lot of force (Ilton, et al., 2018, Science; Patek, 2015, American Scientist; Patek, 2019, ICB). For example, mantis shrimp have a reputation for omnipotence, with their bullet-like strikes, implosive collapse of cavitation bubbles, and stunning ability to fracture hard shells with lightweight hammers (Cox, et al., 2014, Bioinspiration & Biomimetics; deVries, et al., 2012, J. Exp. Biol.; Patek and Caldwell, 2005, J. Exp. Biol.; Patek, et al., 2004, Nature; Patek, et al., 2007, J. Exp. Biol.). However, the fastest mantis shrimp have evolved two-fold slower and more forcefully-contracting muscles than their slower-moving relatives (Blanco and Patek, 2014, Evolution; deVries, et al., 2012, J. Exp. Biol.; McHenry, et al., 2016, J. Exp. Biol.). A force-modified muscle can perform more work to load more potent springs and enable the mantis shrimp’s striking appendage to move more quickly (Patek, et al., 2013, J. Exp. Biol.; Rosario and Patek, 2015, J. Morph.; Zack, et al., 2009, J. Exp. Biol.). In other words, the shift to extremely fast, spring-based actuation requires slowly-contracting, high force muscles – the opposite of what one might expect from a fast system. A constraint of being fast thus becomes apparent: a slow, pre-loaded system limits the ability of animals to rapidly respond to and pursue prey, such that ultrafast systems are not well-suited for pursuit locomotion.
Therefore, muscles are an important part of fast movement, but springs actually enable power amplification. Our research explores the evolutionary biomechanics of springs, with discoveries that explain evolutionary variation in muscles used for loading springs (Blanco and Patek, 2014, Evolution), evolutionary biomechanics of energy storage (Patek, et al., 2013, J. Exp. Biol.; Rosario, et al., 2016, Proc. Royal Society B: Biol. Sci.; Zack, et al., 2009, J. Exp. Biol.), principles of biological spring geometry (Rosario and Patek, 2015, J. Morph.), power limits in springs and latches (Ilton, et al., 2018, Science), and the limits and technical measurements of spring dynamics (Ilton, et al., In review).
Substantial tradeoffs accompany latch-mediated spring actuation (LaMSA) movement. For example, once an animal has evolved an ultrafast movement, sometimes the movements are so brief that they are undetectable by the nervous system, meaning that animals may not be able to adjust the movement once it begins. We discovered that the fastest mantis shrimp adjust spring loading prior to striking and thereby vary the velocity of the strike (Kagaya and Patek, 2016, J. Exp. Biol.). Mantis shrimp have evolved effective strategies for fracturing a range of snail shell shapes and implement these strategies through behaviors before the shell-breaking strike occurs (Cox, et al., 2014, Bioinspiration & Biomimetics; Crane, et al., 2018, J. Exp. Biol.).
Given such tradeoffs, why would mantis shrimp and other organisms evolve ultrafast systems? Potent accelerations and impacts enable mantis shrimp to process food that is otherwise the exclusive purview of much larger animals. Amazingly, cigar-sized mantis shrimp can generate peak forces equivalent to an alligator. Trap-jaw ants can knock out the defenses of their prey before the prey’s nervous system can respond. These and other studies open new doors into the evolutionary ecology of snail shell defenses, predator-prey interactions, the ecology of size, and the behavioral strategies that accompany extreme, spring-driven movement.