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...
SUMMARYRajiform locomotion in fishes is dominated by distinctive undulations of expanded pectoral fins. Unlike other fishes, which typically interact with the fluid environment via multiple fins, undulating rays modulate a single control surface, the pectoral disc, to perform pelagic locomotion, maneuvering and other behaviors. Complex deformations of the broad, flexible pectoral fins occur as the undulating wave varies in three dimensions; pectoral fin kinematics and changes in waveform with swimming speed cannot be fully quantified by two-dimensional analyses of the fin margin. We present the first three-dimensional analysis of undulatory rajiform locomotion in a batoid, the freshwater stingray Potamotrygon orbignyi. Using three cameras (250framess -1 ), we gathered three-dimensional excursion data from 31 points on the pectoral fin during swimming at 1.5 and 2.5disclengthss -1 , describing the propulsive wave and contrasting waveforms between swimming speeds. Only a relatively small region of the pectoral fin (~25%) undulates with significant amplitude (>0.5cm). Stingrays can maintain extreme lateral curvature of the distal fin margin in opposition to induced hydrodynamic loads, ʻcuppingʼ the edge of the pectoral fin into the flow, with potential implications for drag reduction. Wave amplitude increases across both anteroposterior and mediolateral fin axes. Along the anteroposterior axis, amplitude increases until the wave reaches mid-disc and then remains constant, in contrast to angulliform patterns of continuous amplitude increase. Increases in swimming speed are driven by both wave frequency and wavespeed, though multivariate analyses reveal a secondary role for amplitude. Supplementary material available online at
Stingrays, in contrast with many other aquatic animals, have flattened disk-shaped bodies with expanded pectoral 'wings', which are used for locomotion in water. To discover the key features of stingray locomotion, large-eddy simulations of a self-propelled stingray, modelled closely after the freshwater stingray, Potamotrygon orbignyi, are performed. The stingray's body motion was prescribed based on three-dimensional experimental measurement of wing and body kinematics in live stingrays at two different swimming speeds of 1.5 and 2.5L s −1 (L is the disk length of the stingray). The swimming speeds predicted by the self-propelled simulations were within 12 % of the nominal swimming speeds in the experiments. It was found that the fast-swimming stingray (Reynolds number Re = 23 000 and Strouhal number St = 0.27) is approximately 12 % more efficient than the slow-swimming one (Re = 13 500, St = 0.34). This is related to the wake of the fast-and slow-swimming stingrays, which was visualized along with the pressure on the stingray's body. A horseshoe vortex was discovered to be present at the anterior margin of the stingray, creating a low-pressure region that enhances thrust for both fast and slow swimming speeds. Furthermore, it was found that a leading-edge vortex (LEV) on the pectoral disk of swimming stingrays generates a low-pressure region in the fast-swimming stingray, whereas the low-and high-pressure regions in the slow-swimming one are in the back half of the wing and not close to any vortical structures. The undulatory motion creates thrust by accelerating the adjacent fluid (the added-mass mechanism), which is maximized in the back of the wing because of higher undulations and velocities in the back. However, the thrust enhancement by the LEV occurs in the front portion of the wing. By computing the forces on the front half and the back half of the wing, it was found that the contribution of the back half of the wing to thrust in a slow-swimming stingray is several-fold higher than in the fast-swimming one. This indicates that the LEV enhances thrust in fast-swimming stingrays and improves the efficiency of swimming.
Although eyes are generally considered necessary for image resolution, a diffuse photoreceptive system with directional sensitivity may also have this ability. Two species of the echinoid genus Echinometra were tested for spatial vision by examining their ability to locate and move towards targets of different sizes. The echinoids were significantly oriented (P<0.0001) towards a target with an angular width of 33°(0.3·sr) but were not oriented to targets with angular widths of 26°and 16°. This ability is probably due to the blocking of off-angle light by the spines, which have approximately the correct spacing for the observed resolution. Spatial vision is advantageous for echinoids of this genus because they leave and return to small dark shelters. This first demonstration of spatial vision in an echinoderm sheds further light on the complex optical structures and photobehaviors found in this phylum.
Studies of aquatic locomotion typically assume that organisms move through unbounded fluid. However, benthic fishes swim close to the substrate and will experience significant ground effects, which will be greatest for fishes with wide spans such as benthic batoids and flatfishes. Ground effects on fixed-wing flight are well understood, but these models are insufficient to describe the dynamic interactions between substrates and undulating, oscillating fish. Live fish alter their swimming behavior in ground effect, complicating comparisons of near-ground and freestream swimming performance. In this study, a simple, stingray-inspired physical model offers insights into ground effects on undulatory swimmers, contrasting the self-propelled swimming speed, power requirements, and hydrodynamics of fins swimming with fixed kinematics near and far from a solid boundary. Contrary to findings for gliding birds and other fixed-wing fliers, ground effect does not necessarily enhance the performance of undulating fins. Under most kinematic conditions, fins do not swim faster in ground effect, power requirements increase, and the cost of transport can increase by up to 10%. The influence of ground effect varies with kinematics, suggesting that benthic fish might modulate their swimming behavior to minimize locomotor penalties and incur benefits from swimming near a substrate.
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