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.

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.

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.

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.

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.

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.

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.

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.

Developing Biohybrid Robotic Jellyfish (Aurelia aurita) for Free-swimming Tests in the Laboratory and in the Field.

Biohybrid robotics is a growing field that incorporates both live tissues and engineered materials to build robots that address current limitations in robots, including high power consumption and low damage tolerance. One approach is to use microelectronics to enhance whole organisms, which has previously been achieved to control the locomotion of insects. However, the robotic control of jellyfish swimming offers additional advantages, with the potential to become a new ocean monitoring tool in conjunction with existing technologies. Here, we delineate protocols to build a self-contained swim controller using commercially available microelectronics, embed the device into live jellyfish, and calculate vertical swimming speeds in both laboratory conditions and coastal waters. Using these methods, we previously demonstrated enhanced swimming speeds up to threefold, compared to natural jellyfish swimming, in laboratory and in situ experiments. These results offered insights into both designing low-power robots and probing the structure-function of basal organisms. Future iterations of these biohybrid robotic jellyfish could be used for practical applications in ocean monitoring.

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.

Field Testing of Biohybrid Robotic Jellyfish to Demonstrate Enhanced Swimming Speeds.

Biohybrid robotic designs incorporating live animals and self-contained microelectronic systems can leverage the animals' own metabolism to reduce power constraints and act as natural chassis and actuators with damage tolerance. Previous work established that biohybrid robotic jellyfish can exhibit enhanced speeds up to 2.8 times their baseline behavior in laboratory environments. However, it remains unknown if the results could be applied in natural, dynamic ocean environments and what factors can contribute to large animal variability. Deploying this system in the coastal waters of Massachusetts, we validate and extend prior laboratory work by demonstrating increases in jellyfish swimming speeds up to 2.3 times greater than their baseline, with absolute swimming speeds up to 6.6 ± 0.3 cm s-1. These experimental swimming speeds are predicted using a hydrodynamic model with morphological and time-dependent input parameters obtained from field experiment videos. The theoretical model can provide a basis to choose specific jellyfish with desirable traits to maximize enhancements from robotic manipulation. With future work to increase maneuverability and incorporate sensors, biohybrid robotic jellyfish can potentially be used to track environmental changes in applications for ocean monitoring.

The role of suction thrust in the metachronal paddles of swimming invertebrates.

An abundance of swimming animals have converged upon a common swimming strategy using multiple propulsors coordinated as metachronal waves. The shared kinematics suggest that even morphologically and systematically diverse animals use similar fluid dynamic relationships to generate swimming thrust. We quantified the kinematics and hydrodynamics of a diverse group of small swimming animals who use multiple propulsors, e.g. limbs or ctenes, which move with antiplectic metachronal waves to generate thrust. Here we show that even at these relatively small scales the bending movements of limbs and ctenes conform to the patterns observed for much larger swimming animals. We show that, like other swimming animals, the propulsors of these metachronal swimmers rely on generating negative pressure along their surfaces to generate forward thrust (i.e., suction thrust). Relying on negative pressure, as opposed to high pushing pressure, facilitates metachronal waves and enables these swimmers to exploit readily produced hydrodynamic structures. Understanding the role of negative pressure fields in metachronal swimmers may provide clues about the hydrodynamic traits shared by swimming and flying animals.

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.

Maneuvering Performance in the Colonial Siphonophore, Nanomia bijuga.

The colonial cnidarian, Nanomia bijuga, is highly proficient at moving in three-dimensional space through forward swimming, reverse swimming and turning. We used high speed videography, particle tracking, and particle image velocimetry (PIV) with frame rates up to 6400 s-1 to study the kinematics and fluid mechanics of N. bijuga during turning and reversing. N. bijuga achieved turns with high maneuverability (mean length-specific turning radius, R/L = 0.15 ± 0.10) and agility (mean angular velocity, ω = 104 ± 41 deg. s-1). The maximum angular velocity of N. bijuga, 215 deg. s-1, exceeded that of many vertebrates with more complex body forms and neurocircuitry. Through the combination of rapid nectophore contraction and velum modulation, N. bijuga generated high speed, narrow jets (maximum = 1063 ± 176 mm s-1; 295 nectophore lengths s-1) and thrust vectoring, which enabled high speed reverse swimming (maximum = 134 ± 28 mm s-1; 37 nectophore lengths s-1) that matched previously reported forward swimming speeds. A 1:1 ratio of forward to reverse swimming speed has not been recorded in other swimming organisms. Taken together, the colonial architecture, simple neurocircuitry, and tightly controlled pulsed jets by N. bijuga allow for a diverse repertoire of movements. Considering the further advantages of scalability and redundancy in colonies, N. bijuga is a model system for informing underwater propulsion and navigation of complex environments.

Hydrodynamics of Vortex Generation during Bell Contraction by the Hydromedusa Eutonina indicans (Romanes, 1876).

Swimming bell kinematics and hydrodynamic wake structures were documented during multiple pulsation cycles of a Eutonina indicans (Romanes, 1876) medusa swimming in a predominantly linear path. Bell contractions produced pairs of vortex rings with opposite rotational sense. Analyses of the momentum flux in these wake structures demonstrated that vortex dynamics related directly to variations in the medusa swimming speed. Furthermore, a bulk of the momentum flux in the wake was concentrated spatially at the interfaces between oppositely rotating vortices rings. Similar thrust-producing wake structures have been described in models of fish swimming, which posit vortex rings as vehicles for energy transport from locations of body bending to regions where interacting pairs of opposite-sign vortex rings accelerate the flow into linear propulsive jets. These findings support efforts toward soft robotic biomimetic propulsion.

A ctenophore (comb jelly) employs vortex rebound dynamics and outperforms other gelatinous swimmers.

Gelatinous zooplankton exhibit a wide range of propulsive swimming modes. One of the most energetically efficient is the rowing behaviour exhibited by many species of schyphomedusae, which employ vortex interactions to achieve this result. Ctenophores (comb jellies) typically use a slow swimming, cilia-based mode of propulsion. However, species within the genus Ocyropsis have developed an additional propulsive strategy of rowing the lobes, which are normally used for feeding, in order to rapidly escape from predators. In this study, we used high-speed digital particle image velocimetry to examine the kinematics and fluid dynamics of this rarely studied propulsive mechanism. This mechanism allows Ocyropsis to achieve size-adjusted speeds that are nearly double those of other large gelatinous swimmers. The investigation of the fluid dynamic basis of this escape mode reveals novel vortex interactions that have not previously been described for other biological propulsion systems. The arrangement of vortices during escape swimming produces a similar configuration and impact as that of the well-studied 'vortex rebound' phenomenon which occurs when a vortex ring approaches a solid wall. These results extend our understanding of how animals use vortex-vortex interactions and provide important insights that can inform the bioinspired engineering of propulsion systems.

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.