The bodies and brains of fish have evolved to achieve control objectives beyond the capabilities of current underwater vehicles. One route toward designing underwater vehicles with similar capabilities is to better understand fish physiological design and control strategies. This paper has two objectives: 1) to review clues to artificial swimmer design taken from fish physiology and 2) to formalize and review the control problems that must be solved by a robot fish. The goal is to exploit fish locomotion principles to address the truly difficult control challenges of station keeping under large perturbations, rapid maneuvering, power-efficient endurance swimming, and trajectory planning and tracking. The design and control of biomimetic swimming machines meeting these challenges will require state-of-the-art engineering and biology.

Mechanics and control of swimming: a review

Knowledge of the structure–property–function relationships of dermal scales of armoured fish could enable pathways to improved bioinspired human body armour, and may provide clues to the evolutionary origins of mineralized tissues. Here, we present a multiscale experimental and computational approach that reveals the materials design principles present within individual ganoid scales from the ‘living fossil’ Polypterus senegalus. This fish belongs to the ancient family Polypteridae, which first appeared 96 million years ago during the Cretaceous period and still retains many of their characteristics. The mechanistic origins of penetration resistance (approximating a biting attack) were investigated and found to include the juxtaposition of multiple distinct reinforcing composite layers that each undergo their own unique deformation mechanisms, a unique spatial functional form of mechanical properties with regions of differing levels of gradation within and between material layers, and layers with an undetectable gradation, load-dependent effective material properties, circumferential surface cracking, orthogonal microcracking in laminated sublayers and geometrically corrugated junctions between layers. The scales of a fish are its first level of defence. Now, the multilayered structure of fish scales has been analysed according to its mechanical properties and penetration resistance. This study of the four different layers provides a mechanistic understanding of evolutionary design as well as inspiring new materials for armour protection.

http://web.mit.edu/cortiz/www/Ben/nmat2231-rev.pdf

Materials design principles of ancient fish armour

Fish inhabit environments greatly varying in intensity of water velocity, and these flow regimes are generally believed to be of major evolutionary significance. To what extent does water flow drive repeatable and predictable phenotypic differentiation? Although many investigators have examined phenotypic variation across flow gradients in fishes, no clear consensus regarding the nature of water velocity's effects on phenotypic diversity has yet emerged. Here, I describe a generalized model that produces testable hypotheses of morphological and locomotor differentiation between flow regimes in fishes. The model combines biomechanical information (describing how fish morphology determines locomotor abilities) with ecological information (describing how locomotor performance influences fitness) to yield predictions of divergent natural selection and phenotypic differentiation between low-flow and high-flow environments. To test the model's predictions of phenotypic differentiation, I synthesized the existing literature and conducted a meta-analysis. Based on results gathered from 80 studies, providing 115 tests of predictions, the model produced some accurate results across both intraspecific and interspecific scales, as differences in body shape, caudal fin shape, and steady-swimming performance strongly matched predictions. These results suggest that water flow drives predictable phenotypic variation in disparate groups of fish based on a common, generalized model, and that microevolutionary processes might often scale up to generate broader, interspecific patterns. However, too few studies have examined differentiation in body stiffness, muscle architecture, or unsteady-swimming performance to draw clear conclusions for those traits. The analysis revealed that, at the intraspecific scale, both genetic divergence and phenotypic plasticity play important roles in phenotypic differentiation across flow regimes, but we do not yet know the relative importance of these two sources of phenotypic variation. Moreover, while major patterns within and between species were predictable, we have little direct evidence regarding the role of water flow in driving speciation or generating broad, macroevolutionary patterns, as too few studies have addressed these topics or conducted analyses within a phylogenetic framework. Thus, flow regime does indeed drive some predictable phenotypic outcomes, but many questions remain unanswered. This study establishes a general model for predicting phenotypic differentiation across flow regimes in fishes, and should help guide future studies in fruitful directions, thereby enhancing our understanding of the predictability of phenotypic variation in nature.

Predictability of phenotypic differentiation across flow regimes in fishes

Saving energy and enhancing performance are secular preoccupations shared by both nature and human beings. In animal locomotion, flapping flyers or swimmers rely on the flexibility of their wings or body to passively increase their efficiency using an appropriate cycle of storing and releasing elastic energy. Despite the convergence of many observations pointing out this feature, the underlying mechanisms explaining how the elastic nature of the wings is related to propulsive efficiency remain unclear. Here we use an experiment with a self-propelled simplified insect model allowing to show how wing compliance governs the performance of flapping flyers. Reducing the description of the flapping wing to a forced oscillator model, we pinpoint different nonlinear effects that can account for the observed behavior—in particular a set of cubic nonlinearities coming from the clamped-free beam equation used to model the wing and a quadratic damping term representing the fluid drag associated to the fast flapping motion. In contrast to what has been repeatedly suggested in the literature, we show that flapping flyers optimize their performance not by especially looking for resonance to achieve larger flapping amplitudes with less effort, but by tuning the temporal evolution of the wing shape (i.e., the phase dynamics in the oscillator model) to optimize the aerodynamics.

https://www.pnas.org/content/pnas/108/15/5964.full.pdf

Rather than resonance, flapping wing flyers may play on aerodynamics to improve performance

Differences in predation intensity experienced by organisms can lead to divergent natural selection, driving evolutionary change. Western mosquitofish (Gambusia affinis) exhibit larger caudal regions and higher burst-swimming capabilities when coexisting with higher densities of predatory fish. It is hypothesized that a trade-off between steady (constant-speed cruising; important for acquiring resources) and unsteady (rapid bursts and turns; important for escaping predators) locomotion, combined with divergent selection on locomotor performance (favouring steady swimming in high-competition scenarios of low-predation environments, but unsteady swimming in high-predation localities) has caused such phenotypic divergence. Here, I found that morphological differences had a strong genetic basis, and low-predation fish required less hydromechanical power during steady swimming, leading to increased endurance. I further found individual-level support for cause-and-effect relationships between morphology, swimming kinematics and endurance. Results indicate that mosquitofish populations inhabiting low-predation environments have evolved increased steady-swimming abilities via stiffer bodies, larger anterior body/head regions, smaller caudal regions and greater three-dimensional streamlining.

/pdf/trade-off-between-steady-and-unsteady-swimming-underlies-vomwdeojuy.pdf

Trade-off between steady and unsteady swimming underlies predator-driven divergence in Gambusia affinis.

During steady swimming in fish, the dynamic form taken by the axial undulatory wave may depend on the bending stiffness of the body. Previous studies have suggested the hypothesis that fish use their muscles to modulate body stiffness. In order to expand the theoretical and experimental tools available for testing this hypothesis, we explored the relationship between body stiffness, muscle activity, and undulatory waveform in the mechanical context of dynamically bending beams. We propose that fish minimize the mechanical cost of bending by increasing their body stiffness, which would allow them to tune their body's natural frequency to match the tailbeat frequency at a given swimming speed. A review of the literature reveals that the form of the undulatory wave, as measured by propulsive wavelength, is highly variable within species, a result which calls into question the use of propulsive wavelength as a species-specific indicator of swimming mode. At the same time, the smallest wavelength within a species is inversely proportional to the number of vertebrae across taxa ( r 2 = 0.21). In order to determine if intact fish bodies are capable of increasing bending stiffness, we introduce a method for stimulating muscle in the body of a dead fish while it is being cyclically bent at physiological frequencies. The bending moment (N m) and angular displacement (radians) are measured during dynamic bending with and without muscle stimulation. Initial results from these whole body work loops demonstrate that largemouth bass possess the capability to increase body stiffness by using their muscles to generate negative mechanical work.

Karen S. Nipper

Papers

The Importance of Body Stiffness in Undulatory Propulsion