Ontogenetic transitions, biomechanical trade-offs and macroevolution of scyphozoan medusae swimming patterns.

Ephyrae, the early stages of scyphozoan jellyfish, possess a conserved morphology among species. However, ontogenetic transitions lead to morphologically different shapes among scyphozoan lineages, with important consequences for swimming biomechanics, bioenergetics and ecology. We used high-speed imaging to analyse biomechanical and kinematic variables of swimming in 17 species of Scyphozoa (1 Coronatae, 8 "Semaeostomeae" and 8 Rhizostomeae) at different developmental stages. Swimming kinematics of early ephyrae were similar, in general, but differences related to major lineages emerged through development. Rhizostomeae medusae have more prolate bells, shorter pulse cycles and higher swimming performances. Medusae of "Semaeostomeae", in turn, have more variable bell shapes and most species had lower swimming performances. Despite these differences, both groups travelled the same distance per pulse suggesting that each pulse is hydrodynamically similar. Therefore, higher swimming velocities are achieved in species with higher pulsation frequencies. Our results suggest that medusae of Rhizostomeae and "Semaeostomeae" have evolved bell kinematics with different optimized traits, rhizostomes optimize rapid fluid processing, through faster pulsations, while "semaeostomes" optimize swimming efficiency, through longer interpulse intervals that enhance mechanisms of passive energy recapture.

"Indirect development" increases reproductive plasticity and contributes to the success of scyphozoan jellyfish in the oceans.

Ecologists and evolutionary biologists have been looking for the key(s) to the success of scyphomedusae through their long evolutionary history in multiple habitats. Their ability to generate young medusae (ephyrae) via two distinct reproductive strategies, strobilation or direct development from planula into ephyra without a polyp stage, has been a potential explanation. In addition to these reproductive modes, here we provide evidence of a third ephyral production which has been rarely observed and often confused with direct development from planula into ephyra. Planulae of Aurelia relicta Scorrano et al. 2017 and Cotylorhiza tuberculata (Macri 1778) settled and formed fully-grown polyps which transformed into ephyrae within several days. In distinction to monodisk strobilation, the basal polyp of indirect development was merely a non-tentaculate stalk that dissolved shortly after detachment of the ephyra. We provide a fully detailed description of this variant that increases reproductive plasticity within scyphozoan life cycles and is different than either true direct development or the monodisk strobilation. Our observations of this pattern in co-occurrence with mono- and polydisk strobilation in Aurelia spp. suggest that this reproductive mode may be crucial for the survival of some scyphozoan populations within the frame of a bet-hedging strategy and contribute to their long evolutionary success throughout the varied conditions of past and future oceans.

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 most efficient metazoan swimmer creates a 'virtual wall' to enhance performance.

It has been well documented that animals (and machines) swimming or flying near a solid boundary get a boost in performance. This ground effect is often modelled as an interaction between a mirrored pair of vortices represented by a true vortex and an opposite sign 'virtual vortex' on the other side of the wall. However, most animals do not swim near solid surfaces and thus near body vortex-vortex interactions in open-water swimmers have been poorly investigated. In this study, we examine the most energetically efficient metazoan swimmer known to date, the jellyfish Aurelia aurita, to elucidate the role that vortex interactions can play in animals that swim away from solid boundaries. We used high-speed video tracking, laser-based digital particle image velocimetry (dPIV) and an algorithm for extracting pressure fields from flow velocity vectors to quantify swimming performance and the effect of near body vortex-vortex interactions. Here, we show that a vortex ring (stopping vortex), created underneath the animal during the previous swim cycle, is critical for increasing propulsive performance. This well-positioned stopping vortex acts in the same way as a virtual vortex during wall-effect performance enhancement, by helping converge fluid at the underside of the propulsive surface and generating significantly higher pressures which result in greater thrust. These findings advocate that jellyfish can generate a wall-effect boost in open water by creating what amounts to a 'virtual wall' between two real, opposite sign vortex rings. This explains the significant propulsive advantage jellyfish possess over other metazoans and represents important implications for bio-engineered propulsion systems.

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.

Widespread utilization of passive energy recapture in swimming medusae.

Recently, it has been shown that some medusae are capable of swimming very efficiently, i.e. with a low cost of transport, and that this is in part due to passive energy recapture (PER) which occurs during bell relaxation. We compared the swimming kinematics among a diverse array of medusae, varying in taxonomy, morphology and propulsive and foraging modes, in order to evaluate the prevalence of PER in medusae. We found that while PER was common among taxa, the magnitude of the contribution to overall swimming varied greatly. The ability of medusae to utilize PER was not related to morphology and swimming performance but was controlled by their swimming kinematics. Utilizing PER required the medusae to pause after bell expansion and individuals could modulate their PER by changing their pause duration. PER can greatly enhance swimming efficiency but there appear to be trade-offs associated with utilizing PER.

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.

Control of vortex rings for manoeuvrability.

Manoeuvrability is critical to the success of many species. Selective forces acting over millions of years have resulted in a range of capabilities currently unmatched by machines. Thus, understanding animal control of fluids for manoeuvring has both biological and engineering applications. Within inertial fluid regimes, propulsion involves the formation and interaction of vortices to generate thrust. We use both volumetric and planar imaging techniques to quantify how jellyfish (Aurelia aurita) modulate vortex rings during turning behaviour. Our results show that these animals distort individual vortex rings during turns to alter the force balance across the animal, primarily through kinematic modulation of the bell margin. We find that only a portion of the vortex ring separates from the body during turns, which may increase torque. Using a fluorescent actin staining method, we demonstrate the presence of radial muscle fibres lining the bell along the margin. The presence of radial muscles provides a mechanistic explanation for the ability of scyphomedusae to alter their bell kinematics to generate non-symmetric thrust for manoeuvring. These results illustrate the advantage of combining imaging methods and provide new insights into the modulation and control of vorticity for low-speed animal manoeuvring.

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.

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.