Fishes moving through turbulent flows or in formation are regularly exposed to vortices. Although animals living in fluid environments commonly capture energy from vortices, experimental data on the hydrodynamics and neural control of interactions between fish and vortices are lacking. We used quantitative flow visualization and electromyography to show that trout will adopt a novel mode of locomotion to slalom in between experimentally generated vortices by activating only their anterior axial muscles. Reduced muscle activity during vortex exploitation compared with the activity of fishes engaged in undulatory swimming suggests a decrease in the cost of locomotion and provides a mechanism to understand the patterns of fish distributions in schools and riverine environments.

Inspired by the relatively simple morphological blueprint provided by batoid fish such as stingrays and skates, we create a biohybrid system that enables an artificial animal, a tissue-engineered ray, * Correspondence to: K.K.P. 29 Oxford Street, Pierce Hall Cambridge, MA 02130. kkparker@seas.harvard.edu. Phone: 617-495-2850, 617-835-5920. Fax: 617-496-1793 Bioinspired design, as applied to robotics, aims at implementing naturally occurring features such as soft materials, morphologies, gaits, and control mechanisms in artificial settings to improve performance (1-4). For example, recent soft-robotics studies raised awareness on the importance of material properties (3, 4), shifting the focus from rigid elements to soft materials, while other investigations report successful mimicry of gaits or morphological features inspired by insects (5, 6), fish (7,8), snake (9), salamanders (10) and cheetahs (11). While recent advances have the promise of bridging the performance gap with animals, the current soft-robotic actuators based on, for instance, electroactive polymers, shape memory alloys or pressurized fluids, are yet to mature to the point of replicating the high-resolution complex movements of biological muscles (3, 4).In this context, biosensors and bioactuators (12) are intriguing alternatives, since they can intrinsically respond to a number of control inputs (such as electric fields and optical stimulation). Thanks to recent advances in genetic tools (13) and tissue engineering (12), these responses can be altered and tuned across a wide range of time and length scales. Some pioneering studies have exploited these technologies for self-propulsion, developing miniaturized walking machines (14-16), and flagellar (17) or jellyfish inspired (18) swimming devices. These biohybrid systems operate at high energy efficiency and harvest power from energy dense, locally available nutrients, although at present they require specialized environments (physiological solutions) that may limit their applicability. Moreover and most importantly, these biohybrid locomotors lack of the reflexive control (9, 19) necessary to enable adaptive maneuvering and thus of the ability to respond to spatiotemporally varying external stimuli.Here, we design, build and test a tissue-engineered analog of a batoid fish such as stingrays and skates. By combining soft materials and tissue engineering with optogenetics, we created an integrated sensory-motor system that allowed for coordinated undulating fin movement and phototactically controlled locomotion, that is guided via light stimuli. We drew from fish morphology, neuromuscular dynamics and gait control to implement a living, bio-hybrid system that leads to robust and reproducible locomotion and turning maneuvers. Batoid fish are ideal biological models in robotics (8) because their nearly planar bauplan is characterized by a broad dorsoventral disk, with a flattened body and extended pectoral fins, that enhances stability against roll (20). They swim with high energy efficien...

Carangiform swimmers typically have a narrow caudal peduncle, which probably allows them to separate thrust from drag both spatially and temporally. Eels seem to lack this separation, which may explain why they produce a wake with little downstream momentum while carangiform swimmers produce a wake with a clear thrust signature.

What mechanisms of flow control do animals use to enhance hydrodynamic performance? Animals are capable of manipulating flow around the body and appendages both passively and actively. Passive mechanisms rely on structural and morphological components of the body (i.e., humpback whale tubercles, riblets). Active flow control mechanisms use appendage or body musculature to directly generate wake flow structures or stiffen fins against external hydrodynamic loads. Fish can actively control fin curvature, displacement, and area. The vortex wake shed by the tail differs between eel-like fishes and fishes with a discrete narrowing of the body in front of the tail, and three-dimensional effects may play a major role in determining wake structure in most fishes.

SUMMARYMost fishes commonly experience unsteady flows and hydrodynamic perturbations during their lifetime. In this study, we provide evidence that rainbow trout Oncorhynchus mykiss voluntarily alter their body kinematics when interacting with vortices present in the environment that are not self-generated. To demonstrate this, we measured axial swimming kinematics in response to changes in known hydrodynamic wake characteristics. We compared trout swimming in the Kármán street behind different diameter cylinders (2.5 and 5 cm) at two flow speeds (2.5 and 4.5 Ls-1, where L is total body length) to trout swimming in the free stream and in the cylinder bow wake. Trout swimming behind cylinders adopt a distinctive, previously undescribed pattern of movement in order to hold station, which we term the Kármán gait. During this gait,body amplitudes and curvatures are much larger than those of trout swimming at an equivalent flow velocity in the absence of a cylinder. Tail-beat frequency is not only lower than might be expected for a trout swimming in the reduced flow behind a cylinder, but also matches the vortex shedding frequency of the cylinder. Therefore, in addition to choosing to be in the slower flow velocity offered behind a cylinder (drafting), trout are also altering their body kinematics to synchronize with the shed vortices (tuning), using a mechanism that may not involve propulsive locomotion. This behavior is most distinctive when cylinder diameter is large relative to fish length. While tuning, trout have a longer body wavelength than the prescribed wake wavelength, indicating that only certain regions of the body may need to be oriented in a consistent manner to the oncoming vortices. Our results suggest that fish can capture energy from vortices generated by the environment to maintain station in downstream flow. Interestingly, trout swimming in front of a cylinder display lower tail-beat amplitudes and body wave speeds than trout subjected to any of the other treatments, implying that the bow wake may be the most energetically favorable region for a fish to hold station near a cylinder.

The comparative functional anatomy of feeding in Polypterus senegalus, Lepisosteus oculatus, and Amia calva, three primitive actinopterygian fishes, was studied by high-speed cinematography (200 frames per second) synchronized with electromyographic recordings of cranial muscle activity. Several characters of the feeding mechanism have been identified as primitive for actinopterygian fishes: (1) Mandibular depression is mediated by the sternohyoideus muscle via the hyoid apparatus and mandibulohyoid ligament. (2) The obliquus inferioris and sternohyoideus muscles exhibit synchronous activity at the onset of the expansive phase of jaw movement. (3) Activity in the adductor operculi occurs in a double burst pattern-an initial burst at the onset of the expansive phase, followed by a burst after the jaws have closed. (4) A median septum divides the sternohyoideus muscle into right and left halves which are asymmetrically active during chewing and manipulation of prey. (5) Peak hyoid depression occurs only after peak gape has been reached and the hyoid apparatus remains depressed after the jaws have closed. (6) The neurocranium is elevated by the epaxial muscles during the expansive phase. (7) The adductor mandibulae complex is divided into three major sections-an anterior (suborbital) division, a medial division, and a posterolateral division. In Polypterus, the initial strike lasts from 60 to 125 msec, and no temporal overlap in muscle activity occurs between muscles active at the onset of the expansive phase (sternohyoideus, obliquus superioris, epaxial muscles) and the jaw adductors of the compressive phase. In Lepisosteus, the strike is extremely rapid, often occuring in as little as 20 msec. All cranial muscles become active within 10 msec of each other, and there is extensive overlap in muscle activity periods. Two biomechanically independent mechanisms mediate mandibular depression in Amia, and this duality in mouth-opening couplings is a shared feature of the halecostome fishes. Mandibular depression by hyoid retraction, and intermandibular musculature, consisting of an intermandibularis posterior and interhyoideus, are hypothesized to be primitive for the Teleostomi.

Although the functional properties of shark skin have been of considerable interest to both biologists and engineers because of the complex hydrodynamic effects of surface roughness, no study to date has successfully fabricated a flexible biomimetic shark skin that allows detailed study of hydrodynamic function. We present the first study of the design, fabrication and hydrodynamic testing of a synthetic, flexible, shark skin membrane. A three-dimensional (3D) model of shark skin denticles was constructed using micro-CT imaging of the skin of the shortfin mako (Isurus oxyrinchus). Using 3D printing, thousands of rigid synthetic shark denticles were placed on flexible membranes in a controlled, linear-arrayed pattern. This flexible 3D printed shark skin model was then tested in water using a robotic flapping device that allowed us to either hold the models in a stationary position or move them dynamically at their self-propelled swimming speed. Compared with a smooth control model without denticles, the 3D printed shark skin showed increased swimming speed with reduced energy consumption under certain motion programs. For example, at a heave frequency of 1.5 Hz and an amplitude of ±1 cm, swimming speed increased by 6.6% and the energy cost-of-transport was reduced by 5.9%. In addition, a leadingedge vortex with greater vorticity than the smooth control was generated by the 3D printed shark skin, which may explain the increased swimming speeds. The ability to fabricate synthetic biomimetic shark skin opens up a wide array of possible manipulations of surface roughness parameters, and the ability to examine the hydrodynamic consequences of diverse skin denticle shapes present in different shark species.

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