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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.

 

Ctenophores coordinate large macrociliary structures called ctenes to propel themselves through the water. The morphology and kinematics of the ctenes mediate swimming performance. We investigated morphological and kinematic factors affecting swimming performance in free‐swimming ctenophores (Pleurobrachia bachei) using high speed videography. Our morphological results showed that the relationship between body size and ctene morphology and arrangement inP. bacheiwere well described using linear (i.e., isometric) relationships, which suggests functional limitations of ctenes that vary among individuals of different sizes. Our kinematic results showed that isometric constraints on swimming performance can potentially be overcome by alterations in kinematics: (a) swimming speed inP. bacheiincreased with ctene beat frequency over a range of body lengths, and (b) the separation of ctenes into clumps of cilia allowed the ctene to increase in width during the effective stroke and decrease in width during recovery. Separation increases the surface area of the ctene during the effective stroke, likely increasing the thrust produced. The finding that ctenes are not monoliths and instead are separated into clumps of cilia has not been previously described, and we subsequently observed this trait in three other ctenophore species:Euplokamis dunlapae,Bolinopsis infundibulum,andBeroe mitrata. Flexibility in function may be a necessary corollary to isometric development of the ctenes as propulsive structures.

 

Abstract 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. 

Behavioral measurements of fragile aquatic organisms require specialized in situ techniques.We developed an in situ brightfield camera set-up for use during SCUBA diving in aquatic ecosystems.The system uses brightfield illumination with collimated light and an underwater camera to highlight morphological details, body motion and interactions between organisms with high spatial (4K: 3840x2160 pixels) and temporal resolution (up to 120 fps).This technique is particularly useful for gelatinous organisms because of their large (centimeters in length), transparent bodies.Further, the measurements are not subject to experimental artifacts produced in laboratory studies.This method is useful for anyone seeking detailed brightfield images of organisms or nonliving material (e.g. marine snow) in the natural environment. 

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 jellyfishCassiopeasp. plays a significant role with respect to biogenic contributions to water column mixing within its shallow natural habitat ($<2$m deep). The mixing contribution was determined by high-resolution flow velocimetry methods in both the laboratory and the natural environment. We demonstrate thatCassiopeasp. 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^-1for 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 foundCassiopeasp. are capable of releasing porewater into the water column at an average rate of 2.64 mL⋅h⁻¹per individual. The release of nutrient-rich benthic porewater combined with strong contributions to water column mixing suggests a role forCassiopeasp. as an ecosystem engineer in mangrove habitats.

 

ABSTRACT 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. 

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. 

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 engineering of 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. Expected final online publication date for the Annual Review of Marine Science, Volume 13 is January 3, 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates. 

Turning maneuvers by aquatic animals are essential for fundamental life functions such as finding food or mates while avoiding predation. However, turning requires resolution of a fundamental dilemma based in rotational mechanics: the force powering a turn (torque) is favored by an expanded body configuration that maximizes lever arm length, yet minimizing the resistance to a turn (the moment of inertia) is favored by a contracted body configuration. How do animals balance these opposing demands? Here, we directly measure instantaneous forces along the bodies of two animal models—the radially symmetric Aurelia aurita jellyfish, and the bilaterally symmetric Danio rerio zebrafish—to evaluate their turning dynamics. Both began turns with a small, rapid shift in body kinematics that preceded major axial rotation. Although small in absolute magnitude, the high fluid accelerations achieved by these initial motions generated powerful pressure gradients that maximized torque at the start of a turn. This pattern allows these animals to initially maximize torque production before major body curvature changes. Both animals then subsequently minimized the moment of inertia, and hence resistance to axial rotation, by body bending. This sequential solution provides insight into the advantages of re-arranging mass by bending during routine swimming turns.