In an effort to understand the locomotion dynamics of a simple vertebrate, the lamprey, both physical and computational models have been developed. A key feature of these models is the ability to vary the passive stiffness of portions of the swimmer, focusing on highly flexible models similar in material properties to lampreys and other anguilliform fishes. The physical model is a robotic lampreylike swimmer that is actuated along most of its length but has passively flexible tails of different stiffnesses. The computational model is a two-dimensional model that captures fluid-structure interactions using an immersed boundary framework. This simulated lamprey is passively flexible throughout its length and is also actuated along most of its length by the activation of muscle forces. Although the three-dimensional robot and the two-dimensional computational swimmer are such different constructs, we demonstrate that the wake structures generated by these models share many features and we examine how flexibility affects these features. Both models produce wakes with two or more same-sign vortices shed each time the tail changes direction (a “2P” or higher-order wake). In general, wakes become less coherent as tail flexibility increases. We examine the pressure distribution near the tail tip and the timing of vortex formation in both cases and find good agreement. Because we include flexibility, we are able to estimate resonant frequencies for several of the robotic and computational swimmers. We find that actuation at the resonant frequency dramatically increases the distance traveled per tail-beat cycle with only a small increase in the lost kinetic energy in the wake, suggesting that the resonant swimmers are more efficient.

The anterior body of many fishes is shaped like an airfoil turned on its side. With an oscillating angle to the swimming direction, such an airfoil experiences negative pressure due to both its shape and pitching movements. This negative pressure acts as thrust forces on the anterior body. Here, we apply a high-resolution, pressure-based approach to describe how two fishes, bluegill sunfish (Lepomis macrochirusRafinesque) and brook trout (Salvelinus fontinalisMitchill), swimming in the carangiform mode, the most common fish swimming mode, generate thrust on their anterior bodies using leading-edge suction mechanics, much like an airfoil. These mechanics contrast with those previously reported in lampreys—anguilliform swimmers—which produce thrust with negative pressure but do so through undulatory mechanics. The thrust produced on the anterior bodies of these carangiform swimmers through negative pressure comprises 28% of the total thrust produced over the body and caudal fin, substantially decreasing the net drag on the anterior body. On the posterior region, subtle differences in body shape and kinematics allow trout to produce more thrust than bluegill, suggesting that they may swim more effectively. Despite the large phylogenetic distance between these species, and differences near the tail, the pressure profiles around the anterior body are similar. We suggest that such airfoil-like mechanics are highly efficient, because they require very little movement and therefore relatively little active muscular energy, and may be used by a wide range of fishes since many species have appropriately shaped bodies.

Fish use multiple sensory systems, including vision and their lateral line system, to maintain position and speed within a school. Although previous studies have shown that ablating the lateral line alters schooling behavior, no one has examined how the behavior recovers as the sensory system regenerates. We studied how schooling behavior changes in giant danios Devario aequipinnatus when their lateral line system is chemically ablated and after the sensory hair cells regenerate. We found that fish could school normally immediately after chemical ablation, but that they had trouble schooling one to two weeks after the chemical treatment, when the hair cells had fully regenerated. We filmed groups of giant danios with two high-speed cameras and reconstructed the 3D positions of each fish within a group. One fish in the school was treated with gentamycin to ablate all hair cells. Both types of neuromasts, canal and superficial, were completely ablated after treatment but fully regenerated after one week. We quantified the structure of the school using nearest neighbor distance, bearing, elevation, and the cross-correlation of velocity between each pair of fish. Treated fish maintained a normal position within the school immediately after the lateral line ablation, but could not school normally one or two weeks after treatment, even though the neuromasts had fully regenerated. By four to eight weeks post-treatment, the treated fish could again school normally. These results demonstrate that the behavioral recovery after lateral line ablation is a longer process than the regeneration of the hair cells themselves.

Unlike most manmade machines, animals move through their world using flexible bodies and appendages, which bend due to internal muscle and body forces, and also due to forces from the environment. Fishes in particular must cope with fluid dynamic forces that not only resist their overall swimming movements but also may have unsteady flow patterns, vortices, and turbulence, many of which occur more rapidly than what the nervous system can process. Has natural selection led to mechanical properties of fish bodies and their component tissues that can respond very quickly to environmental perturbations? Here, we focus on the mechanical properties of isolated muscle tissue and of the entire intact body in the silver lamprey, Ichthyomyzon unicuspis. We developed two modified work loop protocols to determine the effect of small perturbations on the whole body and on isolated segments of muscle as a function of muscle activation and phase within the swimming cycle. First, we examined how the mechanical properties of the whole lamprey body change depending on the timing of muscle activity. Relative to passive muscle, muscle activation can modulate the effective stiffness by about two-fold and modulate the effective damping by >10-fold depending on the activation phase. Next, we performed a standard work loop test on small sections of axial musculature while adding low-amplitude sinusoidal perturbations at specific frequencies. We modeled the data using a new system identification technique based on time-periodic system analysis and harmonic transfer functions (HTFs) and used the resulting models to predict muscle function under novel conditions. We found that the effective stiffness and damping of muscle varies during the swimming cycle, and that the timing of activation can alter both the magnitude and timing of peak stiffness and damping. Moreover, the response of the isolated muscle was highly nonlinear and length dependent, but the body’s response was much more linear. We applied the resulting HTFs from our experiments to explore the effect of pairs of antagonistic muscles. The results suggest that when muscles work against each other as antagonists, the combined system has weaker nonlinearities than either muscle segment alone. Together, these results begin to provide an integrative understanding of how activation timing can tune the mechanical response properties of muscles, enabling fish to swim effectively in their complex and unpredictable environment.

Nearly all fish have flexible bodies that bend as a result of internal muscular forces and external fluid forces that are dynamically coupled with the mechanical properties of the body. Swimming is therefore strongly influenced by the body's flexibility, yet we do not know how fish species vary in their flexibility and in their ability to modulate flexibility with muscle activity. A more fundamental problem is our lack of knowledge about how any of these differences in flexibility translate into swimming performance. Thus, flexibility represents a hidden axis of diversity among fishes that may have substantial impacts on swimming performance. Although engineers have made substantial progress in understanding these fluid–structure interactions using physical and computational models, the last biological review of these interactions and how they give rise to fish swimming was carried out more than 20 years ago. In this Review, we summarize work on passive and active body mechanics in fish, physical models of fish and bioinspired robots. We also revisit some of the first studies to explore flexural stiffness and discuss their relevance in the context of more recent work. Finally, we pose questions and suggest future directions that may help reveal important links between flexibility and swimming performance.