Distributed propulsion enables fast and efficient swimming modes in physonect siphonophores.

Many fishes employ distinct swimming modes for routine swimming and predator escape. These steady and escape swimming modes are characterized by dramatically differing body kinematics that lead to context-adaptive differences in swimming performance. Physonect siphonophores, such as Nanomia bijuga, are colonial cnidarians that produce multiple jets for propulsion using swimming subunits called nectophores. Physonect siphonophores employ distinct routine and steady escape behaviors but-in contrast to fishes-do so using a decentralized propulsion system that allows them to alter the timing of thrust production, producing thrust either synchronously (simultaneously) for escape swimming or asynchronously (in sequence) for routine swimming. The swimming performance of these two swimming modes has not been investigated in siphonophores. In this study, we compare the performances of asynchronous and synchronous swimming in N. bijuga over a range of colony lengths (i.e., numbers of nectophores) by combining experimentally derived swimming parameters with a mechanistic swimming model. We show that synchronous swimming produces higher mean swimming speeds and greater accelerations at the expense of higher costs of transport. High speeds and accelerations during synchronous swimming aid in escaping predators, whereas low energy consumption during asynchronous swimming may benefit N. bijuga during vertical migrations over hundreds of meters depth. Our results also suggest that when designing underwater vehicles with multiple propulsors, varying the timing of thrust production could provide distinct modes directed toward speed, efficiency, or acceleration.

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.

Nectophore coordination and kinematics by physonect siphonophores.

Siphonophores are ubiquitous and often highly abundant members of pelagic ecosystems throughout the open ocean. They are unique among animal taxa in that many species use multiple jets for propulsion. Little is known about the kinematics of the individual jets produced by nectophores (the swimming bells of siphonophores) or whether the jets are coordinated during normal swimming behavior. Using remotely operated vehicles and SCUBA, we video recorded the swimming behavior of several physonect species in their natural environment. The pulsed kinematics of the individual nectophores that comprise the siphonophore nectosome were quantified and, based on these kinematics, we examined the coordination of adjacent nectophores. We found that, for the five species considered, nectophores located along the same side of the nectosomal axis (i.e. axially aligned) were coordinated and their timing was offset such that they pulsed metachronally. However, this level of coordination did not extend across the nectosome and no coordination was evident between nectophores on opposite sides of the nectosomal axis. For most species, the metachronal contraction waves of nectophores were initiated by the apical nectophores and traveled dorsally. However, the metachronal wave of Apolemia rubriversa traveled in the opposite direction. Although nectophore groups on opposite sides of the nectosome were not coordinated, they pulsed with similar frequencies. This enabled siphonophores to maintain relatively linear trajectories during swimming. The timing and characteristics of the metachronal coordination of pulsed jets affects how the jet wakes interact and may provide important insight into how interacting jets may be optimized for efficient propulsion.

A fundamental propulsive mechanism employed by swimmers and flyers throughout the animal kingdom.

Even casual observations of a crow in flight or a shark swimming demonstrate that animal propulsive structures bend in patterned sequences during movement. Detailed engineering studies using controlled models in combination with analysis of flows left in the wakes of moving animals or objects have largely confirmed that flexibility can confer speed and efficiency advantages. These studies have generally focused on the material properties of propulsive structures (propulsors). However, recent developments provide a different perspective on the operation of nature's flexible propulsors, which we consider in this Commentary. First, we discuss how comparative animal mechanics have demonstrated that natural propulsors constructed with very different material properties bend with remarkably similar kinematic patterns. This suggests that ordering principles beyond basic material properties govern natural propulsor bending. Second, we consider advances in hydrodynamic measurements demonstrating suction forces that dramatically enhance overall thrust produced by natural bending patterns. This is a previously unrecognized source of thrust production at bending surfaces that may dominate total thrust production. Together, these advances provide a new mechanistic perspective on bending by animal propulsors operating in fluids - either water or air. This shift in perspective offers new opportunities for understanding animal motion as well as new avenues for investigation into engineered designs of vehicles operating in fluids.

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.

Swimming kinematics and performance of spinal transected lampreys with different levels of axon regeneration.

Axon regeneration is critical for restoring neural function after spinal cord injury. This has prompted a series of studies on the neural and functional recovery of lampreys after spinal cord transection. Despite this, there are still many basic questions remaining about how much functional recovery depends on axon regeneration. Our goal was to examine how swimming performance is related to degree of axon regeneration in lampreys recovering from spinal cord transection by quantifying the relationship between swimming performance and percent axon regeneration of transected lampreys after 11 weeks of recovery. We found that while swimming speeds varied, they did not relate to percent axon regeneration. In fact, swimming speeds were highly variable within individuals, meaning that most individuals could swim at both moderate and slow speeds, regardless of percent axon regeneration. However, none of the transected individuals were able to swim as fast as the control lampreys. To swim fast, control lampreys generated high amplitude body waves with long wavelengths. Transected lampreys generated body waves with lower amplitude and shorter wavelengths than controls, and to compensate, transected lampreys increased their wave frequencies to swim faster. As a result, transected lampreys had significantly higher frequencies than control lampreys at comparable swimming velocities. These data suggest that the control lampreys swam more efficiently than transected lampreys. In conclusion, there appears to be a minimal recovery threshold in terms of percent axon regeneration required for lampreys to be capable of swimming; however, there also seems to be a limit to how much they can behaviorally recover.

Cool your jets: biological jet propulsion in marine invertebrates.

Pulsatile jet propulsion is a common swimming mode used by a diverse array of aquatic taxa from chordates to cnidarians. This mode of locomotion has interested both biologists and engineers for over a century. A central issue to understanding the important features of jet-propelling animals is to determine how the animal interacts with the surrounding fluid. Much of our knowledge of aquatic jet propulsion has come from simple theoretical approximations of both propulsive and resistive forces. Although these models and basic kinematic measurements have contributed greatly, they alone cannot provide the detailed information needed for a comprehensive, mechanistic overview of how jet propulsion functions across multiple taxa, size scales and through development. However, more recently, novel experimental tools such as high-speed 2D and 3D particle image velocimetry have permitted detailed quantification of the fluid dynamics of aquatic jet propulsion. Here, we provide a comparative analysis of a variety of parameters such as efficiency, kinematics and jet parameters, and review how they can aid our understanding of the principles of aquatic jet propulsion. Research on disparate taxa allows comparison of the similarities and differences between them and contributes to a more robust understanding of aquatic jet propulsion.

Propulsive design principles in a multi-jet siphonophore.

Coordination of multiple propulsors can provide performance benefits in swimming organisms. Siphonophores are marine colonial organisms that orchestrate the motion of multiple swimming zooids for effective swimming. However, the kinematics at the level of individual swimming zooids (nectophores) have not been examined in detail. We used high-speed, high-resolution microvideography and particle image velocimetry of the physonect siphonophore Nanomia bijuga to study the motion of the nectophores and the associated fluid motion during jetting and refilling. The integration of nectophore and velum kinematics allow for a high-speed (maximum ∼1 m s-1), narrow (1-2 mm) jet and rapid refill, as well as a 1:1 ratio of jetting to refill time. Scaled to the 3 mm nectophore length, jet speeds reach >300 lengths s-1 Overall swimming performance is enhanced by velocity gradients produced in the nectophore during refill, which lead to a high-pressure region that produces forward thrust. Generating thrust during both the jet and refill phases augments the distance traveled by 17% over theoretical animals, which generate thrust only during the jet phase. The details of velum kinematics and associated fluid mechanics elucidate how siphonophores effectively navigate three-dimensional space, and could be applied to exit flow parameters in multijet underwater vehicles.

Thrust generation during steady swimming and acceleration from rest in anguilliform swimmers.

Escape swimming is a crucial behavior by which undulatory swimmers evade potential threats. The hydrodynamics of escape swimming have not been well studied, particularly for anguilliform swimmers, such as the sea lamprey Petromyzon marinus For this study, we compared the kinematics and hydrodynamics of larval sea lampreys with those of lampreys accelerating from rest during escape swimming. We used experimentally derived velocity fields to calculate pressure fields and distributions of thrust and drag along the body. Lampreys initiated acceleration from rest with the formation of a high-amplitude body bend at approximately one-quarter body length posterior to the head. This deep body bend produced two high-pressure regions from which the majority of thrust for acceleration was derived. In contrast, steady swimming was characterized by shallower body bends and negative-pressure-derived thrust, which was strongest near the tail. The distinct mechanisms used for steady swimming and acceleration from rest may reflect the differing demands of the two behaviors. High-pressure-based mechanisms, such as the one used for acceleration from rest, could also be important for low-speed maneuvering during which drag-based turning mechanisms are less effective. The design of swimming robots may benefit from the incorporation of such insights from unsteady swimming.

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.

How the bending kinematics of swimming lampreys build negative pressure fields for suction thrust.

Swimming animals commonly bend their bodies to generate thrust. For undulating animals such as eels and lampreys, their bodies bend in the form of waves that travel from head to tail. These kinematics accelerate the flow of adjacent fluids, which alters the pressure field in a manner that generates thrust. We used a comparative approach to evaluate the cause-and-effect relationships in this process by quantifying the hydrodynamic effects of body kinematics at the body-fluid interface of the lamprey, Petromyzon marinus, during steady-state swimming. We compared the kinematics and hydrodynamics of healthy control lampreys to lampreys whose spinal cord had been transected mid-body, resulting in passive kinematics along the posterior half of their body. Using high-speed particle image velocimetry (PIV) and a method for quantifying pressure fields, we detail how the active bending kinematics of the control lampreys were crucial for setting up strong negative pressure fields (relative to ambient fields) that generated high-thrust regions at the bends as they traveled all along the body. The passive kinematics of the transected lamprey were only able to generate significant thrust at the tail, relying on positive pressure fields. These different pressure and thrust scenarios are due to differences in how active versus passive body waves generated and controlled vorticity. This demonstrates why it is more effective for undulating lampreys to pull, rather than push, themselves through the fluid.

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.

Ontogenetic propulsive transitions by Sarsia tubulosa medusae.

While swimming in their natural environment, marine organisms must successfully forage, escape from predation, and search for mates to reproduce. In the process, planktonic organisms interact with their fluid environment, generating fluid signatures around their body and in their downstream wake through ontogeny. In the early stages of their life cycle, marine organisms operate in environments where viscous effects dominate and govern physical processes. Ontogenetic propulsive transitions in swimming organisms often involve dramatic changes in morphology and swimming behavior. However, for organisms that do not undergo significant changes in morphology, swimming behavior or propulsive mode, how is their swimming performance affected? We investigated the ontogenetic propulsive transitions of the hydromedusa Sarsia tubulosa, which utilizes jet propulsion and possesses a similar bell morphology throughout its life cycle. We used digital particle image velocimetry and high-speed imaging to measure the body kinematics, velocity fields and wake structures induced by swimming S. tubulosa with bell exit diameters from 1 to 10 mm. Our experimental observations revealed three distinct classes of hydrodynamic wakes: elongated vortex rings for 1030 (larger than 2 mm bell exit diameter) and elliptical vortex rings (or leading vortex rings) followed by trailing jets for most instances where Re>100 (larger than 4 or 5 mm bell exit diameter). The relative travel distance and propulsive efficiency remained unchanged throughout ontogeny, and the swimming proficiency and hydrodynamic cost of transport decreased non-linearly.

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.

Spinning and corkscrewing of oceanic macroplankton revealed through in situ imaging.

Helical motion is prevalent in nature and has been shown to confer stability and efficiency in microorganisms. However, the mechanics of helical locomotion in larger organisms (>1 centimeter) remain unknown. In the open ocean, we observed the chain forming salp, Iasis cylindrica, swimming in helices. Three-dimensional imaging showed that helicity derives from torque production by zooids oriented at an oblique orientation relative to the chain axis. Colonies can spin both clockwise and counterclockwise and longer chains (>10 zooids) transition from spinning around a linear axis to a helical swimming path. Propulsive jets are non-interacting and directed at a small angle relative to the axis of motion, thus maximizing thrust while minimizing destructive interactions. Our integrated approach reveals the biomechanical advantages of distributed propulsion and macroscale helical movement.

Stealth predation and the predatory success of the invasive ctenophore Mnemiopsis leidyi.

In contrast to higher metazoans such as copepods and fish, ctenophores are a basal metazoan lineage possessing a relatively narrow set of sensory-motor capabilities. Yet lobate ctenophores can capture prey at rates comparable to sophisticated predatory copepods and fish, and they are capable of altering the composition of coastal planktonic communities. Here, we demonstrate that the predatory success of the lobate ctenophore Mnemiopsis leidyi lies in its use of cilia to generate a feeding current that continuously entrains large volumes of fluid, yet is virtually undetectable to its prey. This form of stealth predation enables M. leidyi to feed as a generalist predator capturing prey, including microplankton (approximately 50 µm), copepods (approximately 1 mm), and fish larvae (>3 mm). The efficacy and versatility of this stealth feeding mechanism has enabled M. leidyi to be notoriously destructive as a predator and successful as an invasive species.

Cooperative hydrodynamics accompany multicellular-like colonial organization in the unicellular ciliate Stentor.

Evolution of multicellularity from early unicellular ancestors is arguably one of the most important transitions since the origin of life1,2. Multicellularity is often associated with higher nutrient uptake3, better defense against predation, cell specialization and better division of labor4. While many single-celled organisms exhibit both solitary and colonial existence3,5,6, the organizing principles governing the transition and the benefits endowed are less clear. Using the suspension-feeding unicellular protist Stentor coeruleus, we show that hydrodynamic coupling between proximal neighbors results in faster feeding flows that depend on the separation between individuals. Moreover, we find that the accrued benefits in feeding current enhancement are typically asymmetric- individuals with slower solitary currents gain more from partnering than those with faster currents. We find that colony-formation is ephemeral in Stentor and individuals in colonies are highly dynamic unlike other colony-forming organisms like Volvox carteri 3. Our results demonstrate benefits endowed by the colonial organization in a simple unicellular organism and can potentially provide fundamental insights into the selective forces favoring early evolution of multicellular organization.

Quantifying the feeding behavior and trophic impact of a widespread oceanic ctenophore.

Oceanic ctenophores are widespread predators on pelagic zooplankton. While data on coastal ctenophores often show strong top-down predatory impacts in their ecosystems, differing morphologies, prey capture mechanisms and behaviors of oceanic species preclude the use of coastal data to draw conclusion on oceanic species. We used high-resolution imaging methods both in situ and in the laboratory to quantify interactions of Ocyropsis spp. with natural copepod prey. We confirmed that Ocyropsis spp. uses muscular lobe contraction and a prehensile mouth to capture prey, which is unique amongst ctenophores. This feeding mechanism results in high overall capture success whether encountering single or multiple prey between the lobes (71 and 81% respectively). However, multiple prey require several attempts for successful capture whereas single prey are often captured on the first attempt. Digestion of adult copepods takes 44 min at 25 °C and does not vary with ctenophore size. At high natural densities, we estimate that Ocyropsis spp. consume up to 40% of the daily copepod standing stock. This suggests that, when numerous, Ocyropsis spp. can exert strong top-down control on oceanic copepod populations. At more common densities, these animals consume only a small proportion of the daily copepod standing stock. However, compared to data from pelagic fishes and oceanic medusae, Ocyropsis spp. appears to be the dominant copepod predator in this habitat.

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.

Flow structure and transport characteristics of feeding and exchange currents generated by upside-down Cassiopea jellyfish.

Quantifying the flows generated by the pulsations of jellyfish bells is crucial for understanding the mechanics and efficiency of their swimming and feeding. Recent experimental and theoretical work has focused on the dynamics of vortices in the wakes of swimming jellyfish with relatively simple oral arms and tentacles. The significance of bell pulsations for generating feeding currents through elaborate oral arms and the consequences for particle capture are not as well understood. To isolate the generation of feeding currents from swimming, the pulsing kinematics and fluid flow around the benthic jellyfish Cassiopea spp. were investigated using a combination of videography, digital particle image velocimetry and direct numerical simulation. During the rapid contraction phase of the bell, fluid is pulled into a starting vortex ring that translates through the oral arms with peak velocities that can be of the order of 10 cm s(-1). Strong shear flows are also generated across the top of the oral arms throughout the entire pulse cycle. A coherent train of vortex rings is not observed, unlike in the case of swimming oblate medusae such as Aurelia aurita. The phase-averaged flow generated by bell pulsations is similar to a vertical jet, with induced flow velocities averaged over the cycle of the order of 1-10 mm s(-1). This introduces a strong near-horizontal entrainment of the fluid along the substrate and towards the oral arms. Continual flow along the substrate towards the jellyfish is reproduced by numerical simulations that model the oral arms as a porous Brinkman layer of finite thickness. This two-dimensional numerical model does not, however, capture the far-field flow above the medusa, suggesting that either the three-dimensionality or the complex structure of the oral arms helps to direct flow towards the central axis and up and away from the animal.