S. N. Patek

Biomechanics: Deadly strike mechanism of a mantis shrimp

Stomatopods (mantis shrimp) are well known for the feeding appendages they use to smash shells and impale fish. Here we show that the peacock mantis shrimp (Odontodactylus scyllarus) generates an extremely fast strike that requires major energy storage and release, which we explain in terms of a saddle-shaped exoskeletal spring mechanism. High-speed images reveal the formation and collapse of vapour bubbles next to the prey due to swift movement of the appendage towards it, indicating that O. scyllarus may use destructive cavitation forces to damage its prey.

Extreme impact and cavitation forces of a biological hammer: strike forces of the peacock mantis shrimp Odontodactylus scyllarus.

SUMMARY Mantis shrimp are renowned for their unusual method of breaking shells with brief, powerful strikes of their raptorial appendages. Due to the extreme speeds of these strikes underwater, cavitation occurs between their appendages and hard-shelled prey. Here we examine the magnitude and relative contribution of the impact and cavitation forces generated by the peacock mantis shrimp Odontodactylus scyllarus. We present the surprising finding that each strike generates two brief, high-amplitude force peaks, typically 390–480 μs apart. Based on high-speed imaging, force measurements and acoustic analyses, it is evident that the first force peak is caused by the limbs impact and the second force peak is due to the collapse of cavitation bubbles. Peak limb impact forces range from 400 to 1501 N and peak cavitation forces reach 504 N. Despite their small size, O. scyllarus can generate impact forces thousands of times their body weight. Furthermore, on average, cavitation peak forces are 50% of the limbs impact force, although cavitation forces may exceed the limb impact forces by up to 280%. The rapid succession of high peak forces used by mantis shrimp suggests that mantis shrimp use a potent combination of cavitation forces and extraordinarily high impact forces to fracture shells. The stomatopods hammer is fundamentally different from typical shell-crushing mechanisms such as fish jaws and lobster claws, and may have played an important and as yet unexamined role in the evolution of shell form.

VERTEBRAL COLUMN MORPHOLOGY, C-START CURVATURE, AND THE EVOLUTION OF MECHANICAL DEFENSES IN TETRAODONTIFORM FISHES

Maximum body curvature during the initial phase of escape swimming (stage 1 of C-start) was measured in four species of tropical marine fishes. A linear correlation between maximum curvature and number of functional intervertebral joints was found (range for number of joints, 17-25). A biomechanical model of vertebral column bending predicts that, if intervertebral joint angles are held constant, increasing the number of joints should produce a linear decrease in the measured curvature coefficient (curvature coefficient is inversely related to curvature). The measured curvature coefficients fit this model closely, indicating that, within the range of 17-25 joints, vertebral number is an important determinant of vertebral column flexibility. The study species with the lowest vertebral number, a filefish, Monacanthus hispidus, is a member of the Tetraodontiformes, a group characterized by the lowest vertebral numbers found among fishes. Elaborate antipredator defenses, such as a carapace and the ability to inflate the body, have evolved six times within the Tetraodontiformes, and some form of mechanical defense is present in all families of this group. We propose an evolutionary scenario in which low vertebral number reduced the escape swimming performance of ancestral tetraodontiforms, thus increasing their vulnerability to predators and driving the repeated evolution of mechanical defenses in this group. Our finding that lower vertebral numbers are correlated with lower C-start curvature suggests that low vertebral number may impair escape performance; thus, one necessary condition for the proposed scenario is met.

Multifunctionality and mechanical origins: Ballistic jaw propulsion in trap-jaw ants

Extreme animal movements are usually associated with a single, high-performance behavior. However, the remarkably rapid mandible strikes of the trap-jaw ant, Odontomachus bauri, can yield multiple functional outcomes. Here we investigate the biomechanics of mandible strikes in O. bauri and find that the extreme mandible movements serve two distinct functions: predation and propulsion. During predatory strikes, O. bauri mandibles close at speeds ranging from 35 to 64 m·s−1 within an average duration of 0.13 ms, far surpassing the speeds of other documented ballistic predatory appendages in the animal kingdom. The high speeds of the mandibles assist in capturing prey, while the extreme accelerations result in instantaneous mandible strike forces that can exceed 300 times the ant’s body weight. Consequently, an O. bauri mandible strike directed against the substrate produces sufficient propulsive power to launch the ant into the air. Changing head orientation and strike surfaces allow O. bauri to use the trap-jaw mechanism to capture prey, eject intruders, or jump to safety. This use of a single, simple mechanical system to generate a suite of profoundly different behavioral functions offers insights into the morphological origins of novelties in feeding and locomotion.

COMPARATIVE TESTS OF EVOLUTIONARY TRADE‐OFFS IN A PALINURID LOBSTER ACOUSTIC SYSTEM

Abstract Communication structures vary greatly in size and can be structurally and behaviorally integrated with other systems. In structurally integrated systems, dramatic changes in size may impose trade‐offs with the size of neighboring structures. In spiny lobsters (Palinuridae), there is a fivefold difference in size of the antennular plate, on which sound producing apparatus is located, such that the antennular plate reaches 38% carapace length in some sound producers (Stridentes) compared to only 4% carapace length in non‐sound producing spiny lobsters (Silentes). We examined whether this major variation in antennular plate size imposes trade‐offs with the adjoining antennae, specifically in the context that the signal producing structures and antennae are both used in predator defense. We recorded and analyzed lobster sounds in order to test whether size increases in the acoustic morphology were correlated with production of particular signal features. Antennal and antennular plate structures were measured across the family, including both Stridentes and Silentes. Phylogenetic comparative methods were used to test for correlated evolutionary change among the structures and signal features. We analyzed the phylogenetic relationships of the Palinuridae based on morphological characters and ribosomal DNA evidence (16S, 18S and 28S nuclear and mitochondrial ribosomal RNA gene regions). We found that the number of sound pulses was positively correlated with length of the sound producing apparatus. Opposite to the predicted trade‐offs, we found that the size of the antennular plate was positively correlated with size of the surrounding antennae within Stridentes. Nevertheless, when Stridentes were compared to Silentes, the latter had relatively larger antennae for a given antennular plate size than did the sound producing taxa. These results suggest that body size does not limit size increases in acoustic structures within Stridentes, however the presence and associated constructional costs of a sound producing apparatus may impose a trade‐off when taxa with and without the apparatus are compared. Alternatively, since both systems are used in predator defense, this pattern may indicate greater selection for antennal force production in Silentes, which lack the additional acoustic mode of predator defense.

Linkage mechanics and power amplification of the mantis shrimp's strike

SUMMARY Mantis shrimp (Stomatopoda) generate extremely rapid and forceful predatory strikes through a suite of structural modifications of their raptorial appendages. Here we examine the key morphological and kinematic components of the raptorial strike that amplify the power output of the underlying muscle contractions. Morphological analyses of joint mechanics are integrated with CT scans of mineralization patterns and kinematic analyses toward the goal of understanding the mechanical basis of linkage dynamics and strike performance. We test whether a four-bar linkage mechanism amplifies rotation in this system and find that the rotational amplification is approximately two times the input rotation, thereby amplifying the velocity and acceleration of the strike. The four-bar model is generally supported, although the observed kinematic transmission is lower than predicted by the four-bar model. The results of the morphological, kinematic and mechanical analyses suggest a multi-faceted mechanical system that integrates latches, linkages and lever arms and is powered by multiple sites of cuticular energy storage. Through reorganization of joint architecture and asymmetric distribution of mineralized cuticle, the mantis shrimps raptorial appendage offers a remarkable example of how structural and mechanical modifications can yield power amplification sufficient to produce speeds and forces at the outer known limits of biological systems.

From bouncy legs to poisoned arrows: elastic movements in invertebrates

Summary Elastic mechanisms in the invertebrates are fantastically diverse, yet much of this diversity can be captured by examining just a few fundamental physical principles. Our goals for this commentary are threefold. First, we aim to synthesize and simplify the fundamental principles underlying elastic mechanisms and show how different configurations of basic building blocks can be used for different functions. Second, we compare single rapid movements and rhythmic movements across six invertebrate examples – ranging from poisonous cnidarians to high-jumping froghoppers – and identify remarkable functional properties arising from their underlying elastic systems. Finally, we look to the future of this field and find two prime areas for exciting new discoveries – the evolutionary dynamics of elastic mechanisms and biomimicry of invertebrate elastic materials and mechanics.

Sound production during feeding in Hippocampus seahorses (Syngnathidae)

While there have been many anecdotal reports of sounds produced by Hippocampus seahorses, little is known about the mechanisms of sound production. We investigated clicking sounds produced during feeding strikes in H. zosterae and H. erectus. Descriptions of head morphology support the idea that feeding clicks may represent stridulatory sounds produced by a bony articulation between the supraoccipital ridge of the neurocranium and the grooved anterior margin of the coronet. Analysis of high-speed video and synchronous sound recordings of H. erectus indicate that the feeding click begins within 1-2 msec of the onset of the rapid feeding strike (4 msec mean duration). Surgical manipulations of the supraoccipital-coronet articulation resulted in a decreased proportion of feeding strikes that produced clicks. This study provides several lines of evidence in support of the hypothesis that feeding clicks in Hippocampus seahorses are stridulatory in origin and are produced by the supraoccipital-coronet articulation. Our results are not consistent with previous suggestions that sounds may be produced by cavitation due to rapid pressure changes within the buccal cavity during the feeding strike.

MODULARITY AND SCALING IN FAST MOVEMENTS: POWER AMPLIFICATION IN MANTIS SHRIMP

Extremely fast animal actions are accomplished with mechanisms that reduce the duration of movement. This process is known as power amplification. Although many studies have examined the morphology and performance of power‐amplified systems, little is known about their development and evolution. Here, we examine scaling and modularity in the powerful predatory appendages of a mantis shrimp, Gonodactylaceus falcatus (Crustacea, Stomatopoda). We propose that power‐amplified systems can be divided into three units: an engine (e.g., muscle), an amplifier (e.g., spring), and a tool (e.g., hammer). We tested whether these units are developmentally independent using geometric morphometric techniques that quantitatively compare shapes. Additionally, we tested whether shape and several mechanical features are correlated with size and sex. We found that the morphological regions that represent the engine, amplifier, and tool belong to independent developmental modules. In both sexes, body size was positively correlated with the size of each region. Shape, however, changed allometrically with appendage size only in the amplifier (both sexes) and tool (males). These morphological changes were correlated with strike force and spring force (amplifier), but not spring stiffness (amplifier). Overall, the results indicate that each functional unit belongs to different developmental modules in a power‐amplified system, potentially allowing independent evolution of the engine, amplifier, and tool.

Strike mechanics of an ambush predator: the spearing mantis shrimp.

SUMMARY Ambush predation is characterized by an animal scanning the environment from a concealed position and then rapidly executing a surprise attack. Mantis shrimp (Stomatopoda) consist of both ambush predators (‘spearers’) and foragers (‘smashers’). Spearers hide in sandy burrows and capture evasive prey, whereas smashers search for prey away from their burrows and typically hammer hard-shelled, sedentary prey. Here, we examined the kinematics, morphology and field behavior of spearing mantis shrimp and compared them with previously studied smashers. Using two species with dramatically different adult sizes, we found that strikes produced by the diminutive species, Alachosquilla vicina, were faster (mean peak speed 5.72±0.91 m s–1; mean duration 3.26±0.41 ms) than the strikes produced by the large species, Lysiosquillina maculata (mean peak speed 2.30±0.85 m s–1; mean duration 24.98±9.68 ms). Micro-computed tomography and dissections showed that both species have the spring and latch structures that are used in other species for producing a spring-loaded strike; however, kinematic analyses indicated that only A. vicina consistently engages the elastic mechanism. In the field, L. maculata ambushed evasive prey primarily at night while hidden in burrows, striking with both long and short durations compared with laboratory videos. We expected ambush predators to strike with very high speeds, yet instead we found that these spearing mantis shrimp struck more slowly and with longer durations than smashers. Nonetheless, the strikes of spearers occurred at similar speeds and durations to those of other aquatic predators of evasive prey. Although counterintuitive, these findings suggest that ambush predators do not actually need to produce extremely high speeds, and that the very fastest predators are using speed to achieve other mechanical feats, such as producing large impact forces.