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.

Does the settling column method underestimate phytoplankton sinking speeds?

Phytoplankton sinking is a major component of vertical ocean carbon and nutrient fluxes, and sinking is an integral component of phytoplankton biology and ecology. Much of our understanding of phytoplankton sinking derives from the settling column method (SETCOL) in which sinking speeds are calculated from the proportion of cells reaching the bottom of a water-filled column after a set time. Video-based methods are a recent alternative to SETCOL in which sinking speeds are measured by tracking the movement of individual cells in a salinity-stratified water column. In this study, we present the results of a meta-analysis showing that SETCOL produces significantly and consistently lower sinking speeds than the video method. Next, we perform a particle image velocimetry analysis, which shows that the observed discrepancy in sinking speeds between the two methods can probably be explained by weak convection currents in the SETCOLs. Finally, we discuss the implications of these results for the interpretation of past and future phytoplankton sinking speed measurements and models that rely on those measurements.

Fish can use coordinated fin motions to recapture their own vortex wake energy.

During swimming, many fishes use pectoral fins for propulsion and, in the process, move substantial amounts of water rearward. However, the effect that this upstream wake has on the caudal fin remains largely unexplored. By coordinating motions of the caudal fin with the pectoral fins, fishes have the potential to create constructive flow interactions which may act to partially recapture the upstream energy lost in the pectoral fin wake. Using experimentally derived velocity and pressure fields for the silver mojarra (Eucinostomus argenteus), we show that pectoral-caudal fin (PCF) coordination enables the circulation and interception of pectoral fin wake vortices by the caudal fin. This acts to transfer energy to the caudal fin and enhance its hydrodynamic efficiency at swimming speeds where this behaviour occurs. We also find that mojarras commonly use PCF coordination in nature. The results offer new insights into the evolutionary drivers and behavioural plasticity of fish swimming as well as for developing more capable bioinspired underwater vehicles.

The hydrodynamics and kinematics of the appendicularian tail underpin peristaltic pumping.

Planktonic organisms feed while suspended in water using various hydrodynamic pumping strategies. Appendicularians are a unique group of plankton that use their tail to pump water over mucous mesh filters to concentrate food particles. As ubiquitous and often abundant members of planktonic ecosystems, they play a major role in oceanic food webs. Yet, we lack a complete understanding of the fluid flow that underpins their filtration. Using high-speed, high-resolution video and micro particle image velocimetry, we describe the kinematics and hydrodynamics of the tail in Oikopleura dioica in filtering and free-swimming postures. We show that sinusoidal waves of the tail generate peristaltic pumping within the tail chamber with fluid moving parallel to the tail when filtering. We find that the tail contacts attachment points along the tail chamber during each beat cycle, serving to seal the tail chamber and drive pumping. When we tested how the pump performs across environmentally relevant temperatures, we found that the amplitude of the tail was invariant but tail beat frequency increased threefold across three temperature treatments (5°C, 15°C and 25°C). Investigation into this unique pumping mechanism gives insight into the ecological success of appendicularians and provides inspiration for novel pump designs.

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.

Benthic jellyfish act as suction pumps to facilitate release of interstitial porewater.

Upside-down jellyfish, genus Cassiopea (Péron and Lesueur, 1809), are found in shallow coastal habitats in tropical and subtropical regions circumglobally. These animals have previously been demonstrated to produce flow both in the water column as a feeding current, and in the interstitial porewater, where they liberate porewater at rates averaging 2.46 mL h-1. Since porewater in Cassiopea habitat can be nutrient-rich, this is a potential source of nutrient enrichment in these ecosystems. This study experimentally determines that porewater release by Cassiopea sp. jellyfish is due to suction pumping, and not the Bernoulli effect. This suggests porewater release is directly coupled to bell pulsation rate, and unlike vertical jet flux, should be unaffected by population density. In addition, we show that bell pulsation rate is positively correlated with temperature, and negatively correlated with animal size. As such, we would predict an increase in the release of nutrient-rich porewater during the warm summer months. Furthermore, we show that, at our field site in Lido Key, Florida, at the northernmost limit of Cassiopea range, population densities decline during the winter, increasing seasonal differences in porewater release.

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.

A tale of two fish tails: does a forked tail really perform better than a truncate tail when cruising?

Many fishes use their tail as the main thrust producer during swimming. This fin's diversity in shape and size influences its physical interactions with water as well as its ecological functions. Two distinct tail morphologies are common in bony fishes: flat, truncate tails which are best suited for fast accelerations via drag forces, and forked tails that promote economical, fast cruising by generating lift-based thrust. This assumption is based primarily on studies of the lunate caudal fin of Scombrids (i.e. tuna, mackerel), which is comparatively stiff and exhibits an airfoil-type cross-section. However, this is not representative of the more commonly observed and taxonomically widespread flexible forked tail, yet similar assumptions about economical cruising are widely accepted. Here, we present the first comparative experimental study of forked versus truncate tail shape and compare the fluid mechanical properties and energetics of two common nearshore fish species. We examined the hypothesis that forked tails provide a hydrodynamic advantage over truncate tails at typical cruising speeds. Using experimentally derived pressure fields, we show that the forked tail produces thrust via acceleration reaction forces like the truncate tail during cruising but at increased energetic costs. This reduced efficiency corresponds to differences in the performance of the two tail geometries and body kinematics to maintain similar overall thrust outputs. Our results offer insights into the benefits and tradeoffs of two common fish tail morphologies and shed light on the functional morphology of fish swimming to guide the development of bio-inspired underwater technologies.

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.

Benthic jellyfish dominate water mixing in mangrove ecosystems.

Water mixing is a critical mechanism in marine habitats that governs many important processes, including nutrient transport. Physical mechanisms, such as winds or tides, are primarily responsible for mixing effects in shallow coastal systems, but the sheltered habitats adjacent to mangroves experience very low turbulence and vertical mixing. The significance of biogenic mixing in pelagic habitats has been investigated but remains unclear. In this study, we show that the upside-down jellyfish Cassiopea sp. plays a significant role with respect to biogenic contributions to water column mixing within its shallow natural habitat ([Formula: see text] m deep). The mixing contribution was determined by high-resolution flow velocimetry methods in both the laboratory and the natural environment. We demonstrate that Cassiopea sp. continuously pump water from the benthos upward in a vertical jet with flow velocities on the scale of centimeters per second. The volumetric flow rate was calculated to be 212 L⋅h-1 for average-sized animals (8.6 cm bell diameter), which translates to turnover of the entire water column every 15 min for a median population density (29 animals per m2). In addition, we found Cassiopea sp. are capable of releasing porewater into the water column at an average rate of 2.64 mL⋅h-1 per individual. The release of nutrient-rich benthic porewater combined with strong contributions to water column mixing suggests a role for Cassiopea sp. as an ecosystem engineer in mangrove habitats.

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.