Medusan morphospace: phylogenetic constraints, biomechanical solutions, and ecological consequences

Abstract. Medusae were the earliest animals to evolve muscle‐powered swimming in the seas. Although medusae have achieved diverse and prominent ecological roles throughout the world's oceans, we argue that the primitive organization of cnidarian muscle tissue limits force production and, hence, the mechanical alternatives for swimming bell function. We use a recently developed model comparing the potential force production with the hydrodynamic requirements of jet propulsion, and conclude that jet production is possible only at relatively small bell diameters. In contrast, production of a more complex wake via what we term rowing propulsion permits much larger sizes but requires a different suite of morphological features. Analysis of morphometric data from all medusan taxa independently confirms size‐dependent patterns of bell forms that correspond with model predictions. Further, morphospace analysis indicates that various lineages within the Medusozoa have proceeded along either of two evolutionary trajectories. The first alternative involved restriction of jet‐propelled medusan bell diameters to small dimensions. These medusae may be either solitary individuals (characteristic of Anthomedusae and Trachymedusae) or aggregates of small individual medusan units into larger colonial forms (characteristic of the nectophores of many members of the Siphonophorae). The second trajectory involved use of rowing propulsion (characteristic of Scyphozoa and some hydromedusan lineages such as the Leptomedusae and Narcomedusae) that allows much larger bell sizes. Convergence on either of the differing propulsive alternatives within the Medusozoa has emerged via parallel evolution among different medusan lineages. The distinctions between propulsive modes have important ecological ramifications because swimming and foraging are interdependent activities for medusae. Rowing swimmers are characteristically cruising predators that select different prey types from those selected by jet‐propelled medusae, which are predominantly ambush predators. These relationships indicate that the different biomechanical solutions to constraints on bell function have entailed ecological consequences that are evident in the prey selection patterns and trophic impacts of contemporary medusan lineages.     

Propulsion in Cubomedusae: Mechanisms and Utility

Evolutionary constraints which limit the forces produced during bell contractions of medusae affect the overall medusan morphospace such that jet propulsion is limited to only small medusae. Cubomedusae, which often possess large prolate bells and are thought to swim via jet propulsion, appear to violate the theoretical constraints which determine the medusan morphospace. To examine propulsion by cubomedusae, we quantified size related changes in wake dynamics, bell shape, swimming and turning kinematics of two species of cubomedusae, Chironex fleckeri and Chiropsella bronzie. During growth, these cubomedusae transitioned from using jet propulsion at smaller sizes to a rowing-jetting hybrid mode of propulsion at larger sizes. Simple modifications in the flexibility and kinematics of their velarium appeared to be sufficient to alter their propulsive mode. Turning occurs during both bell contraction and expansion and is achieved by generating asymmetric vortex structures during both stages of the swimming cycle. Swimming characteristics were considered in conjunction with the unique foraging strategy used by cubomedusae.     

Ontogenetic changes in the bell morphology and kinematics and swimming behavior of rowing medusae: the special case of the limnomedusa Liriope tetraphylla

Swimming animals may experience significant changes in the Reynolds number (Re) of their surrounding fluid flows throughout ontogeny. Many medusae experience Re environments with significant viscous forces as small juveniles but inertially dominated Re environments as adults. These different environments may affect their propulsive strategies. In particular, rowing, a propulsive strategy with ecological advantages for large adults, may be constrained by viscosity for small juvenile medusae. We examined changes in the bell morphology and swimming kinematics of the limnomedusa Liriope tetraphylla at different stages of development. L. tetraphylla maintained an oblate bell (fineness ratio ≈ 0.5-0.6), large velar aperture ratio (R(v) ≈ 0.5-0.8), and rapid bell kinematics throughout development. These traits enabled it to use rowing propulsion at all stages except the very smallest sizes observed (diameter = 0.14 cm). During the juvenile stage, very rapid bell kinematics served to increase Re sufficiently for rowing propulsion. Other taxa that use rowing propulsion as adults, such as leptomedusae and scyphomedusae, typically utilize different propulsive strategies as small juveniles to function in low Re environments. We compared the performance values of the different propulsive modes observed among juvenile medusae.     

Transitions in morphology, nematocyst distribution, fluid motions, and prey capture during development of the scyphomedusa Cyanea capillata

Like that of most scyphozoans, the ontogeny of Cyanea capillata medusae involves substantive alterations in feeding structures and mechanics. We used video and optical microscopy approaches to quantify these ontogenetic changes in morphology, flow, and feeding of C. capillata medusae. We found that alterations in gross morphology and nematocyst distributions coincided with a shift from prey capture on the manubrium or lappets of ephyrae (bell diameter 0.2-0.4 cm) to capture primarily on the tentacles in adult medusae (diameter >1.0 cm). These changes occurred within a hydrodynamic framework that itself changed due to medusan growth. Viscous forces were important in flows around small ephyrae (maximum Re <10(1)), whereas viscosity was less influential in the inertially dominated flows around adult medusae (Re > 10(2)). The relative timing of these events indicates that ontogenetic processes are closely synchronized with alterations in the hydrodynamic environment within which C. capillata medusae develop.     

Turbulence: does vorticity affect the structure and shape of body and fin propulsors?

Over the past century, many ideas have been developed on the relationships between water flow and the structure and shape of the body and fins of fishes, largely during swimming in relatively steady flows. However, both swimming by fishes and the habitats they occupy are associated with vorticity, typically concentrated as eddies characteristic of turbulent flow. Deployment of methods to examine flow in detail suggests that vorticity impacts the lives of fishes. First, vorticity near the body and fins can increase thrust and smooth variations in thrust that are a consequence of using oscillating and undulating propulsors to swim. Second, substantial mechanical energy is dissipated in eddies in the wake and adaptations that minimize these losses would be anticipated. We suggest that such mechanisms may be found in varying the length of the propulsive wave, stiffening propulsive surfaces, and shifting to using median and paired fins when swimming at low speeds. Eddies in the flow encountered by fishes may be beneficial, but when eddy radii are of the order of 0.25 of the fish's total length, negative impacts occur due to greater difficulties in controlling stability. The archetypal streamlined "fish" shape reduces destabilizing forces for fishes swimming into eddies.     

Field observations of four Aurelia labiata jellyfish behaviours: swimming down in response to low salinity pre-empted swimming up in response to touch,but animal and plant materials were captured equally

Jellyfish live in complex environments and must continually make behavioural choices. In field observations, adult Aurelia labiata were confronted with a conflict between swimming up elicited by touch of the manubrium and swimming down elicited by low salinity. Following a touch, downward-swimming medusae (1.5–2.0 m deep) turned and swam to within 0.5 m of the surface when the salinity in the top 1.5 m of the water column was greater than 20 ppt but medusae uniformly refused to swim up into the top 1.25 m when the salinity was less than 20 ppt even after being touched three times. The central nervous system of A. labiata appears to have neural circuitry that specifies their response when medusae encounter stimuli that elicit incompatible behaviours. Upward-swimming adult medusae had animal, vegetable or cellulose (paper) material dispersed ahead of them. Medusae captured each material on the bell margin and transported it to a gastric pouch. Medusae displayed only minor behavioural differences in the process. Having sensory, neural and muscular systems organized to capture and pass to the stomach, a huge variety of materials allows medusae to survive in different seasons and environments.     

Experimental and Numerical Study of Penguin Mode Flapping Foil Propulsion System for Ships

The use of biomimetic tandem flapping foils for ships and underwater vehicles is considered as a unique and interesting concept in the area of marine propulsion.The flapping wings can be used as a thrust producing,stabilizer and control devices which has both propulsion and maneuvering applications for marine vehicles.In the present study,the hydrodynamic performance of a pair of flexible flapping foils resembling penguin flippers is studied.A ship model of 3 m in length is fitted with a pair of counter flapping foils at its bottom mid-ship region.Model tests are carried out in a towing tank to estimate the propulsive performance of flapping foils in bollard and self propulsion modes.The same tests are performed in a numerical environment using a Computational Fluid Dynamics (CFD) software.The numerical and experimental results show reasonably good agreement in both bollard pull and self propulsion trials.The numerical studies are carried out on flexible flapping hydrofoil in unsteady conditions using moving unstructured grids.The efficiency and force coefficients of the flexible flapping foils are determined and presented as a function of Strouhal number.     

A Biomimetic Approach to Robot Locomotion in Unstructured and Slippery Environments

While much attention has been given to bio-robotics in recent years, not much of this has been given to the challenging subject of locomotion in slippery conditions. This study begins to rectify this by proposing a biomimetic approach to generating the friction required to give sufficient propulsive force on a slippery substrate. We took inspiration from a successful biological solution-that of applying hair-like structures to the propulsive appendages, similar to the setae found in nereid polychaetes living in muddy habitats. We began by examining the morphology and the mean locomotion parameters of one of the most common nereids: Nereis diversicolor. Following this study, we designed and fabricated a robotic system with appendages imitating the biological shape found in the worm. A flexible control system was developed to allow most of the locomotion parameters observed in the real worm to be applied to the robot. Experiments on three different natural substrates ranging from fine sand to gravel showed     

Unsteady Aspects of Aquatic Locomotion

Virtually all animals swim unsteadily. They oscillate appendages,undulate, and produce periodic propulsive forces so that thevelocity of some part of their bodies changes in time. Becauseof their unsteady motion, animals experience a fluid force inaddition to drag—the acceleration reaction. The accelerationreaction dominates the forces resisting rapid accelerationsof animals and may be responsible for generating thrust in oscillatingappendages and undulating bodies. The ever-present unsteadynature of animal swimming implies diverse applications of theacceleration reaction.     

Numerical Study of Propulsion Mechanism for Oscillating Rigid and Flexible Tuna-Tails

Numerical study on the unsteady hydrodynamic characteristics of oscillating rigid and flexible tuna-tails in viscous flow-field is performed.Investigations are conducted using Reynolds-Averaged Navier-Stokes (RANS) equations with a moving adaptive mesh.The effect of swimming speed,flapping amplitude,frequency and flexure amplitude on the propulsion performance of the rigid and flexible tuna-tails are investigated.Computational results reveal that a pair of leading edge vortices develop along the tail surface as it undergoes an oscillating motion.The propulsive efficiency has a strong correlation with various locomotive parameters.Peak propulsive efficiency can be obtained by adjusting these parameters.Particularly,when input power coefficient is less than 2.8,the rigid tail generates larger thrust force and higher propulsive efficiency than flexible tail.However,when input power coefficient is larger than 2.8,flexible tail is superior to rigid tail.     

Flipper bone distribution reveals flexible trailing edge in underwater flying marine tetrapods

Hydrofoil-shaped limbs (flipper-hydrofoils) have evolved independently several times in secondarily marine tetrapods and generally fall into two functional categories: (1) those that produce the majority of thrust during locomotion (propulsive flipper-hydrofoils); (2) those used primarily to steer and resist destabilizing movements such as yaw, pitch, and roll (controller flipper-hydrofoils). The morphological differences between these two types have been poorly understood. Theoretical and experimental studies on engineered hydrofoils suggest that flapping hydrofoils with a flexible trailing edge are more efficient at producing thrust whereas hydrofoils used in steering and stabilization benefit from a more rigid one. To investigate whether the trailing edge is generally more flexible in propulsive flipper-hydrofoils, we compared the bone distribution along the chord in both flipper types. The propulsive flipper-hydrofoil group consists of the forelimbs of Chelonioidea, Spheniscidae, and Otariidae. The controller flipper-hydrofoil group consists of the forelimbs of Cetacea. We quantified bone distribution from radiographs of species representing more than 50% of all extant genera for each clade. Our results show that the proportion of bone in both groups is similar along the leading edge (0–40% of the chord) but is significantly less along the trailing edge for propulsive flipper-hydrofoils (40–80% of the chord). Both flipper-hydrofoil types have little to no bony tissue along the very edge of the trailing edge (80–100% of the chord). This suggests a relatively flexible trailing edge for propulsive flipper-hydrofoils compared to controller flipper-hydrofoils in line with findings from prior studies. This study presents a morphological correlate for inferring flipper-hydrofoil function in extinct taxa and highlights the importance of a flexible trailing edge in the evolution of propulsive flipper-hydrofoils in marine tetrapods.     

A biomimetic robotic jellyfish (Robojelly) actuated by shape memory alloy composite actuators

An analysis is conducted on the design, fabrication and performance of an underwater vehicle mimicking the propulsion mechanism and physical appearance of a medusa (jellyfish). The robotic jellyfish called Robojelly mimics the morphology and kinematics of the Aurelia aurita species. Robojelly actuates using bio-inspired shape memory alloy composite actuators. A systematic fabrication technique was developed to replicate the essential structural features of A. aurita. Robojelly's body was fabricated from RTV silicone having a total mass of 242 g and bell diameter of 164 mm. Robojelly was able to generate enough thrust in static water conditions to propel itself and achieve a proficiency of 0.19 s(-1) while the A. aurita achieves a proficiency of around 0.25 s(-1). A thrust analysis based on empirical measurements for a natural jellyfish was used to compare the performance of the different robotic configurations. The configuration with best performance was a Robojelly with segmented bell and a passive flap structure. Robojelly was found to consume an average power on the order of 17 W with the actuators not having fully reached a thermal steady state.     

Wake Vortex Structure Characteristics of a Flexible Oscillating Fin

We compute the wake of a two-dimensional and three-dimensional flexible fin in an unsteady flow field with heaving and pitching motions using FLUENT. Deflexion mode is used for a non-uniform cantilever beam with non-uniformly distributed load. The effect of chordwise deflexion length on the characteristics of propulsion is discussed for two-dimensional flexible fin. The thrust coefficient decreases, propulsive efficiency increases and the intensity of turbulence attenuates gradually as the deflexion length increases. For a three-dimensional flexible fin, the intensity of the vortex in the plane of symmetry is higher than that in the plane at 3/4 span length of the caudal fin. But the propulsive perform.ance achieved is not what we expected with the given deflexion mode.     

Modes and scaling in aquatic locomotion

Organisms spanning a 10(7)-fold range in length of the body engage in aquatic propulsion-swimming; they do so with several kinds of propulsors and take advantage of several different fluid mechanical mechanisms. A hierarchical classification of swimming modes can impose some order on this complexity. More difficult are the issues surrounding the different kinds of propulsive devices used by different organisms. These issues can be in part exposed by an examination of how speeds and accelerations scale with changes in body length, both for different lineages of swimmers and for all swimmers collectively. Clearly, fluid mechanical factors impose general rules and constraints; just as clearly, these only roughly anticipate actual scaling. Indeed, collections of data on scaling can serve as useful correctives for assumptions about functional mechanisms. They can also reveal size-dependent constraints on biological designs.     

Pedal neuron 3 serves a significant role in effecting turning during crawling by the marine slug <Emphasis Type="Italic">Tritonia diomedea</Emphasis> (Bergh)

The marine nudibranch Tritonia diomedea crawls using its ciliated foot surface as the sole means of propulsion. Turning while crawling involves raising a small portion of the lateral foot margin on the side of the turn. The cilia in the lifted area no longer contribute to propulsion, and this asymmetry in thrust turns the animal towards the lifted side. Neurons located in the pedal ganglia of the brain contribute to these foot margin contractions. T. diomedea has a natural tendency to turn upstream (rheotaxis), and pedal flexion neuron Pedal 3 elicits foot margin lift and receives modulatory input from flow receptors. To assess the contribution of this single cell in turning behavior, two fine wires were glued to the surface of the brain over left and right Pedal 3. We determined that Pedal 3 activity is correlated with subsequent ipsilateral turns, preceding the lift of the foot margin and the change in orientation by a consistent interval. Both Pedal 3 cells show synchronous bursts of activity, and the firing frequency of the ipsilateral Pedal 3 increased before turns were observed to that side. Stimulation of the electrode over Pedal 3 proved sufficient to elicit an ipsilateral turn in Tritonia.     

Morphology of the nematocysts of the medusae of two scyphozoans, Catostylus mosaicus and Phyllorhiza punctata (Rhizostomeae): implications for capture of prey

Abstract. We examined the cnidomes (total complement of nematocysts) of medusae of the zooxanthellate and azooxanthellate jellyfishes Phyllorhiza punctata and Catostylus mosaicus (Rhizostomeae, Scyphozoa), and compared the assemblage of zooplankton captured on the oral arms of each species to determine whether differences in the types or amount of zooplankton captured were consistent with possible differences in the cnidomes. Cnidomes were described using light and scanning electron microscopy. Each species had a distinct cnidome and, in general, specimens of P. punctata appeared to have far fewer nematocysts than those of C. mosaicus. Four types of nematocysts were identified in medusae of C. mosaicus; 2 types of holotrichous isorhizae, rhopaloids, and birhopaloids. In C. mosaicus, the oral arms and bell margins possessed all of these types, but the cnidomes of the 2 regions differed in relative abundances and sizes of isorhizae and rhopaloids. Five types of nematocysts were identified in medusae of P. punctata, although not all types were found in all specimens. Round holotrichous isorhizae were found only in the bell, while oval holotrichous isorhizae, rhopaloids of 2 distinct size ranges, and birhopaloids were found in the bell and oral arms. Cnidomes of the bell and oral arms in specimens of P. punctata also differed in the relative abundance and sizes of oval isorhizae and rhopaloids. Although there were clear differences in the overall cnidomes and absolute abundances of nematocysts in each species, the oral arms (feeding appendages) of specimens of both C. mosaicus and P. punctata had similar types and relative abundances of nematocysts. Zooplankton sampled from the oral arms of each species showed that both species preyed predominantly on copepod nauplii and larvae of gastropods and bivalves. Medusae of C. mosaicus captured ～10 × more gastropod larvae and 5 × more bivalve larvae than those of P. punctata. Specimens of P. punctata captured approximately twice as many copepod nauplii as those of C. mosaicus. Differences in the relative abundance of types of zooplankton captured by each species could not be adequately explained by differences in the cnidomes of the oral arms.     

Go reconfigure: how fish change shape as they swim and evolve

The bodies of fish change shape over propulsive, behavioral, developmental, and evolutionary time scales, a general phenomenon that we call "reconfiguration". Undulatory, postural, and form-reconfiguration can be distinguished, studied independently, and examined in terms of mechanical interactions and evolutionary importance. Using a combination of live, swimming fishes and digital robotic fish that are autonomous and self-propelled, we examined the functional relation between undulatory and postural reconfiguration in forward swimming, backward swimming, and yaw turning. To probe how postural and form reconfiguration interact, the yaw turning of leopard sharks was examined using morphometric and kinematic analyses. To test how undulatory reconfiguration might evolve, the digital robotic fish were subjected to selection for enhanced performance in a simulated ecology in which each individual had to detect and move towards a food source. In addition to the general issue of reconfiguration, these investigations are united by the fact that the dynamics of undulatory and postural reconfigurations are predicted to be determined, in part, by the structural stiffness of the fish's body. Our method defines undulatory reconfiguration as the combined, point-by-point periodic motion of the body, leaving postural reconfiguration as the combined deviations from undulatory reconfiguration. While undulatory reconfiguration appears to be the sole or primary propulsive driver, postural reconfiguration may contribute to propulsion in hagfish and it is correlated with differences in forward, and backward, swimming in lamprey. Form reconfigures over developmental time in leopard sharks in a manner that is consistent with an allometric scaling theory in which structural stiffness of the body is held constant. However, correlation of a form proxy for structural stiffness of the body suggests that body stiffness may scale in order to limit maximum postural reconfiguration during routine yaw turns. When structural stiffness and undulatory frequency are modeled as determining the tail's undulatory wave speed, both factors evolve under selection for enhanced foraging behavior in the digital fish-like robots. The methods used in making these distinctions between kinds of reconfiguration have broad applicability in fish biology, especially for quantifying complex motor behaviors in the wild and for simulating selection on behavior that leads to directional evolution of functional phenotypes.     

Design and Experiments of a Robotic Fish Imitating Cow-Nosed Ray

<正> The cow-nosed ray is studied as natural sample of a flapping-foil robotic fish.Body structure, motion discipline, and dynamicfoil deformation of cow-nosed ray are analyzed.Based on the analysis results, a robotic fish imitating cow-nosed ray,named Robo-ray Ⅱ, mainly composed of soft body, flexible ribs and pneumatic artificial muscles, is developed.Structure andswimming morphology of the robotic prototype are as that of a normal cow-nosed ray in nature.Key propulsion parameters ofRobo-ray Ⅱ at normal conditions, including the St Number at linear swimming, thrust coefficient at towing are studied throughexperiments.The suitable driving parameters are confirmed considering the efficiency and swimming velocity.Swimmingvelocity of 0.16 m·s~(-1)'and thrust coefficient of 0.56 in maximum are achieved in experiments.