Electromechanical enhancement of live jellyfish for ocean exploration.

The vast majority of the ocean's volume remains unexplored, in part because of limitations on the vertical range and measurement duration of existing robotic platforms. In light of the accelerating rate of climate change impacts on the physics and biogeochemistry of the ocean, the need for new tools that can measure more of the ocean on faster timescales is becoming pressing. Robotic platforms inspired or enabled by aquatic organisms have the potential to augment conventional technologies for ocean exploration. Recent work demonstrated the feasibility of directly stimulating the muscle tissue of live jellyfish via implanted microelectronics. We present a biohybrid robotic jellyfish that leverages this external electrical swimming control, while also using a 3D printed passive mechanical attachment to streamline the jellyfish shape, increase swimming performance, and significantly enhance payload capacity. A six-meter-tall, 13 600 l saltwater facility was constructed to enable testing of the vertical swimming capabilities of the biohybrid robotic jellyfish over distances exceeding 35 body diameters. We found that the combination of external swimming control and the addition of the mechanical forebody resulted in an increase in swimming speeds to 4.5 times natural jellyfish locomotion. Moreover, the biohybrid jellyfish were capable of carrying a payload volume up to 105% of the jellyfish body volume. The added payload decreased the intracycle acceleration of the biohybrid robots relative to natural jellyfish, which could also facilitate more precise measurements by onboard sensors that depend on consistent platform motion. While many robotic exploration tools are limited by cost, energy expenditure, and varying oceanic environmental conditions, this platform is inexpensive, highly efficient, and benefits from the widespread natural habitats of jellyfish. The demonstrated performance of these biohybrid robots suggests an opportunity to expand the set of robotic tools for comprehensive monitoring of the changing ocean.

Response to comment on 'A conserved strategy for inducing appendage regeneration in moon jellyfish, Drosophila, and mice'.

Previously we reported evidence that a regenerative response in the appendages of moon jellyfish, fruit flies, and mice can be promoted by nutrient modulation (Abrams et al., 2021). Sustar and Tuthill subsequently reported that they had not been able to reproduce the induced regenerative response in flies (Sustar and Tuthill, 2023). Here we discuss that differences in the amputation method, treatment concentrations, age of the animals, and stress management explain why they did not observe a regenerative response in flies. Typically, 30-50% of treated flies showed response in our assay.

A conserved strategy for inducing appendage regeneration in moon jellyfish, Drosophila, and mice.

Can limb regeneration be induced? Few have pursued this question, and an evolutionarily conserved strategy has yet to emerge. This study reports a strategy for inducing regenerative response in appendages, which works across three species that span the animal phylogeny. In Cnidaria, the frequency of appendage regeneration in the moon jellyfish Aurelia was increased by feeding with the amino acid L-leucine and the growth hormone insulin. In insects, the same strategy induced tibia regeneration in adult Drosophila. Finally, in mammals, L-leucine and sucrose administration induced digit regeneration in adult mice, including dramatically from mid-phalangeal amputation. The conserved effect of L-leucine and insulin/sugar suggests a key role for energetic parameters in regeneration induction. The simplicity by which nutrient supplementation can induce appendage regeneration provides a testable hypothesis across animals.

The ability of animals to replace damaged or lost tissue (or 'regenerate') is a sliding scale, with some animals able to regenerate whole limbs, while others can only scar. But why some animals can regenerate while others have more limited capabilities has puzzled the scientific community for many years. The likes of Charles Darwin and August Weismann suggested regeneration only evolves in a particular organ. In contrast, Thomas Morgan suggested that all animals are equipped with the tools to regenerate but differ in whether they are able to activate these processes. If the latter were true, it could be possible to 'switch on' regeneration. Animals that keep growing throughout their life and do not regulate their body temperatures are more likely to be able to regenerate. But what do growth and temperature regulation have in common? Both are highly energy-intensive, with temperature regulation potentially diverting energy from other processes. A question therefore presents itself: could limb regeneration be switched on by supplying animals with more energy, either in the form of nutrients like sugars or amino acids, or by giving them growth hormones such as insulin? Abrams, Tan, Li et al. tested this hypothesis by amputating the limbs of jellyfish, flies and mice, and then supplementing their diet with sucrose (a sugar), leucine (an amino acid) and/or insulin for eight weeks while they healed. Typically, jellyfish rearrange their remaining arms when one is lost, while fruit flies are not known to regenerate limbs. House mice are usually only able to regenerate the very tip of an amputated digit. But in Abrams, Tan, Li et al.'s experiments, leucine and insulin supplements stimulated limb regeneration in jellyfish and adult fruit flies, and leucine and sucrose supplements allowed mice to regenerate digits from below the second knuckle. Although regeneration was not observed in all animals, these results demonstrate that regeneration can be induced, and that it can be done relatively easily, by feeding animals extra sugar and amino acids. These findings highlight increasing the energy supplies of different animals by manipulating their diets while they are healing from an amputated limb can aid in regeneration. This could in the future pave the way for new therapeutic approaches to tissue and organ regeneration.

Neuromechanical wave resonance in jellyfish swimming.

For organisms to have robust locomotion, their neuromuscular organization must adapt to constantly changing environments. In jellyfish, swimming robustness emerges when marginal pacemakers fire action potentials throughout the bell's motor nerve net, which signals the musculature to contract. The speed of the muscle activation wave is dictated by the passage times of the action potentials. However, passive elastic material properties also influence the emergent kinematics, with time scales independent of neuromuscular organization. In this multimodal study, we examine the interplay between these two time scales during turning. A three-dimensional computational fluid-structure interaction model of a jellyfish was developed to determine the resulting emergent kinematics, using bidirectional muscular activation waves to actuate the bell rim. Activation wave speeds near the material wave speed yielded successful turns, with a 76-fold difference in turning rate between the best and worst performers. Hyperextension of the margin occurred only at activation wave speeds near the material wave speed, suggesting resonance. This hyperextension resulted in a 34-fold asymmetry in the circulation of the vortex ring between the inside and outside of the turn. Experimental recording of the activation speed confirmed that jellyfish actuate within this range, and flow visualization using particle image velocimetry validated the corresponding fluid dynamics of the numerical model. This suggests that neuromechanical wave resonance plays an important role in the robustness of an organism's locomotory system and presents an undiscovered constraint on the evolution of flexible organisms. Understanding these dynamics is essential for developing actuators in soft body robotics and bioengineered pumps.

The Hydrodynamics of Jellyfish Swimming.

Jellyfish have provided insight into important components of animal propulsion, such as suction thrust, passive energy recapture, vortex wall effects, and the rotational mechanics of turning. These traits are critically important to jellyfish because they must propel themselves despite severe limitations on force production imposed by rudimentary cnidarian muscular structures. Consequently, jellyfish swimming can occur only by careful orchestration of fluid interactions. Yet these mechanics may be more broadly instructive because they also characterize processes shared with other animal swimmers, whose structural and neurological complexity can obscure these interactions. In comparison with other animal models, the structural simplicity, comparative energetic efficiency, and ease of use in laboratory experimentation allow jellyfish to serve as favorable test subjects for exploration of the hydrodynamic bases of animal propulsion. These same attributes also make jellyfish valuable models for insight into biomimetic or bioinspired engineeringof swimming vehicles. Here, we review advances in understanding of propulsive mechanics derived from jellyfish models as a pathway toward the application of animal mechanics to vehicle designs.

Suction-based propulsion as a basis for efficient animal swimming.

A central and long-standing tenet in the conceptualization of animal swimming is the idea that propulsive thrust is generated by pushing the surrounding water rearward. Inherent in this perspective is the assumption that locomotion involves the generation of locally elevated pressures in the fluid to achieve the expected downstream push of the surrounding water mass. Here we show that rather than pushing against the surrounding fluid, efficient swimming animals primarily pull themselves through the water via suction. This distinction is manifested in dominant low-pressure regions generated in the fluid surrounding the animal body, which are observed by using particle image velocimetry and a pressure calculation algorithm applied to freely swimming lampreys and jellyfish. These results suggest a rethinking of the evolutionary adaptations observed in swimming animals as well as the mechanistic basis for bio-inspired and biomimetic engineered vehicles.

An algorithm to estimate unsteady and quasi-steady pressure fields from velocity field measurements.

We describe and characterize a method for estimating the pressure field corresponding to velocity field measurements such as those obtained by using particle image velocimetry. The pressure gradient is estimated from a time series of velocity fields for unsteady calculations or from a single velocity field for quasi-steady calculations. The corresponding pressure field is determined based on median polling of several integration paths through the pressure gradient field in order to reduce the effect of measurement errors that accumulate along individual integration paths. Integration paths are restricted to the nodes of the measured velocity field, thereby eliminating the need for measurement interpolation during this step and significantly reducing the computational cost of the algorithm relative to previous approaches. The method is validated by using numerically simulated flow past a stationary, two-dimensional bluff body and a computational model of a three-dimensional, self-propelled anguilliform swimmer to study the effects of spatial and temporal resolution, domain size, signal-to-noise ratio and out-of-plane effects. Particle image velocimetry measurements of a freely swimming jellyfish medusa and a freely swimming lamprey are analyzed using the method to demonstrate the efficacy of the approach when applied to empirical data.

Passive energy recapture in jellyfish contributes to propulsive advantage over other metazoans.

Gelatinous zooplankton populations are well known for their ability to take over perturbed ecosystems. The ability of these animals to outcompete and functionally replace fish that exhibit an effective visual predatory mode is counterintuitive because jellyfish are described as inefficient swimmers that must rely on direct contact with prey to feed. We show that jellyfish exhibit a unique mechanism of passive energy recapture, which is exploited to allow them to travel 30% further each swimming cycle, thereby reducing metabolic energy demand by swimming muscles. By accounting for large interspecific differences in net metabolic rates, we demonstrate, contrary to prevailing views, that the jellyfish (Aurelia aurita) is one of the most energetically efficient propulsors on the planet, exhibiting a cost of transport (joules per kilogram per meter) lower than other metazoans. We estimate that reduced metabolic demand by passive energy recapture improves the cost of transport by 48%, allowing jellyfish to achieve the large sizes required for sufficient prey encounters. Pressure calculations, using both computational fluid dynamics and a newly developed method from empirical velocity field measurements, demonstrate that this extra thrust results from positive pressure created by a vortex ring underneath the bell during the refilling phase of swimming. These results demonstrate a physical basis for the ecological success of medusan swimmers despite their simple body plan. Results from this study also have implications for bioinspired design, where low-energy propulsion is required.

Biomimetic and live medusae reveal the mechanistic advantages of a flexible bell margin.

Flexible bell margins are characteristic components of rowing medusan morphologies and are expected to contribute towards their high propulsive efficiency. However, the mechanistic basis of thrust augmentation by flexible propulsors remained unresolved, so the impact of bell margin flexibility on medusan swimming has also remained unresolved. We used biomimetic robotic jellyfish vehicles to elucidate that propulsive thrust enhancement by flexible medusan bell margins relies upon fluid dynamic interactions between entrained flows at the inflexion point of the exumbrella and flows expelled from under the bell. Coalescence of flows from these two regions resulted in enhanced fluid circulation and, therefore, thrust augmentation for flexible margins of both medusan vehicles and living medusae. Using particle image velocimetry (PIV) data we estimated pressure fields to demonstrate a mechanistic basis of enhanced flows associated with the flexible bell margin. Performance of vehicles with flexible margins was further enhanced by vortex interactions that occur during bell expansion. Hydrodynamic and performance similarities between robotic vehicles and live animals demonstrated that the propulsive advantages of flexible margins found in nature can be emulated by human-engineered propulsors. Although medusae are simple animal models for description of this process, these results may contribute towards understanding the performance of flexible margins among other animal lineages.

A tissue-engineered jellyfish with biomimetic propulsion.

Reverse engineering of biological form and function requires hierarchical design over several orders of space and time. Recent advances in the mechanistic understanding of biosynthetic compound materials, computer-aided design approaches in molecular synthetic biology 4,5 and traditional soft robotics, and increasing aptitude in generating structural and chemical micro environments that promote cellular self-organization have enhanced the ability to recapitulate such hierarchical architecture in engineered biological systems. Here we combined these capabilities in a systematic design strategy to reverse engineer a muscular pump. We report the construction of a freely swimming jellyfish from chemically dissociated rat tissue and silicone polymer as a proof of concept. The constructs, termed 'medusoids', were designed with computer simulations and experiments to match key determinants of jellyfish propulsion and feeding performance by quantitatively mimicking structural design, stroke kinematics and animal-fluid interactions. The combination of the engineering design algorithm with quantitative benchmarks of physiological performance suggests that our strategy is broadly applicable to reverse engineering of muscular organs or simple life forms that pump to survive.

A viscosity-enhanced mechanism for biogenic ocean mixing.

Recent observations of biologically generated turbulence in the ocean have led to conflicting conclusions regarding the significance of the contribution of animal swimming to ocean mixing. Measurements indicate elevated turbulent dissipation--comparable with levels caused by winds and tides--in the vicinity of large populations of planktonic animals swimming together. However, it has also been noted that elevated turbulent dissipation is by itself insufficient proof of substantial biogenic mixing, because much of the turbulent kinetic energy of small animals is injected below the Ozmidov buoyancy length scale, where it is primarily dissipated as heat by the fluid viscosity before it can affect ocean mixing. Ongoing debate regarding biogenic mixing has focused on comparisons between animal wake turbulence and ocean turbulence. Here, we show that a second, previously neglected mechanism of fluid mixing--first described over 50 years ago by Charles Darwin--is the dominant mechanism of mixing by swimming animals. The efficiency of mixing by Darwin's mechanism is dependent on animal shape rather than fluid length scale and, unlike turbulent wake mixing, is enhanced by fluid viscosity. Therefore, it provides a means of biogenic mixing that can be equally effective in small zooplankton and large mammals. A theoretical model for the relative contributions of Darwinian mixing and turbulent wake mixing is created and validated by in situ field measurements of swimming jellyfish using a newly developed scuba-based laser velocimetry device. Extrapolation of these results to other animals is straightforward given knowledge of the animal shape and orientation during vertical migration. On the basis of calculations of a broad range of aquatic animal species, we conclude that biogenic mixing via Darwin's mechanism can be a significant contributor to ocean mixing and nutrient transport.

Fast-swimming hydromedusae exploit velar kinematics to form an optimal vortex wake.

Fast-swimming hydromedusan jellyfish possess a characteristic funnel-shaped velum at the exit of their oral cavity that interacts with the pulsed jets of water ejected during swimming motions. It has been previously assumed that the velum primarily serves to augment swimming thrust by constricting the ejected flow in order to produce higher jet velocities. This paper presents high-speed video and dye-flow visualizations of free-swimming Nemopsis bachei hydromedusae, which instead indicate that the time-dependent velar kinematics observed during the swimming cycle primarily serve to optimize vortices formed by the ejected water rather than to affect the speed of the ejected flow. Optimal vortex formation is favorable in fast-swimming jellyfish because, unlike the jet funnelling mechanism, it allows for the minimization of energy costs while maximizing thrust forces. However, the vortex ;formation number' corresponding to optimality in N. bachei is substantially greater than the value of 4 found in previous engineering studies of pulsed jets from rigid tubes. The increased optimal vortex formation number is attributable to the transient velar kinematics exhibited by the animals. A recently developed model for instantaneous forces generated during swimming motions is implemented to demonstrate that transient velar kinematics are required in order to achieve the measured swimming trajectories. The presence of velar structures in fast-swimming jellyfish and the occurrence of similar jet-regulating mechanisms in other jet-propelled swimmers (e.g. the funnel of squid) appear to be a primary factor contributing to success of fast-swimming jetters, despite their primitive body plans.

Flow patterns generated by oblate medusan jellyfish: field measurements and laboratory analyses.

Flow patterns generated by medusan swimmers such as jellyfish are known to differ according the morphology of the various animal species. Oblate medusae have been previously observed to generate vortex ring structures during the propulsive cycle. Owing to the inherent physical coupling between locomotor and feeding structures in these animals, the dynamics of vortex ring formation must be robustly tuned to facilitate effective functioning of both systems. To understand how this is achieved, we employed dye visualization techniques on scyphomedusae (Aurelia aurita) observed swimming in their natural marine habitat. The flow created during each propulsive cycle consists of a toroidal starting vortex formed during the power swimming stroke, followed by a stopping vortex of opposite rotational sense generated during the recovery stroke. These two vortices merge in a laterally oriented vortex superstructure that induces flow both toward the subumbrellar feeding surfaces and downstream. The lateral vortex motif discovered here appears to be critical to the dual function of the medusa bell as a flow source for feeding and propulsion. Furthermore, vortices in the animal wake have a greater volume and closer spacing than predicted by prevailing models of medusan swimming. These effects are shown to be advantageous for feeding and swimming performance, and are an important consequence of vortex interactions that have been previously neglected.

Sensitivity analysis of kinematic approximations in dynamic medusan swimming models.

Models of medusan swimming typically rely on kinematic approximations to observed animal morphology to make such investigations tractable. The effect of these simplifications on the accuracy of predicted dynamics has not been examined in detail. We conduct a case study of the scyphozoan jellyfish Chrysaora fuscescens to isolate and quantify the sensitivity of dynamic models to common kinematic approximations. It is found that dynamic models exhibit strong dependence on the nature of some approximations and the context in which they are implemented. Therefore it is incorrect and potentially misleading to assume that achieving kinematic similarity in models of measured animal locomotion will necessarily provide dynamically correct models.