John H. Costello

Flow patterns generated by oblate medusan jellyfish: field measurements and laboratory analyses

SUMMARY Flow patterns generated by medusan swimmers such as jellyfish are known to differ according the morphology of the various animal species. Oblate medusae have been previously observed to generate vortex ring structures during the propulsive cycle. Owing to the inherent physical coupling between locomotor and feeding structures in these animals, the dynamics of vortex ring formation must be robustly tuned to facilitate effective functioning of both systems. To understand how this is achieved, we employed dye visualization techniques on scyphomedusae (Aurelia aurita) observed swimming in their natural marine habitat. The flow created during each propulsive cycle consists of a toroidal starting vortex formed during the power swimming stroke, followed by a stopping vortex of opposite rotational sense generated during the recovery stroke. These two vortices merge in a laterally oriented vortex superstructure that induces flow both toward the subumbrellar feeding surfaces and downstream. The lateral vortex motif discovered here appears to be critical to the dual function of the medusa bell as a flow source for feeding and propulsion. Furthermore, vortices in the animal wake have a greater volume and closer spacing than predicted by prevailing models of medusan swimming. These effects are shown to be advantageous for feeding and swimming performance, and are an important consequence of vortex interactions that have been previously neglected.

Morphology, fluid motion and predation by the scyphomedusa Aurelia aurita

Although medusan predators play demonstrably important roles in a variety of marine ecosystems, the mechanics of prey capture and, hence, prey selection, have remained poorly defined. A review of the literature describing the commonly studied medusa Aurelia aurita (Linnaeus 1758) reveals no distinct patterns of prey selectivity and suggests that A. aurita is a generalist and feeds unselectively upon available zooplankton. We examined the mechanics of prey capture by A. aurita using video methods to record body and fluid motions. Medusae were collected between February and June in 1990 and 1991 from Woods Hole, Massachusetts and Narragansett Bay, Rhode Island, USA. Tentaculate A. aurita create fluid motions during swimming which entrain prey and bring them into contact with tentacles. We suggest that this mechanism dominates prey selection by A. aurita. In this case, we predict that medusae of a specific diameter will positively select prey with escape speeds slower than the flow velocities at their bell margins. Negatively selected prey escape faster than the medusan flow velocity draws them to capture surfaces. Faster prey will be captured by larger medusac because flow field velocity is a function of bell diameter. On the basis of prey escape velocities and flow field velocities of A. aurita with diameters of 0.8 to 7.1 cm, we predict that A. aurita will select zooplankton such as barnacle nauplii and some slow swimming hydromedusae, while faster copepods will be negatively selected.

Flow and Feeding by Swimming Scyphomedusae

The mechanical basis of prey capture by scyphomedusae has been largely ignored, despite the importance of these predators in a variety of planktonic ecosystems. Interactions between swimming, fluid motions, and prey capture were examined during 1991–1992 for a species from the three scyphozoan orders having planktonic medusae: Rhizostomeae, Stomolophus meleagris Agassiz, 1862; Coronatae, Linuche unguiculata (Schwartz, 1788); and Semaeostomeae, Cyanea capillata (Linnaeus, 1758). All three species used flow created during bell pulsation to capture prey, but the type of flow used for prey capture and the capture surface morphology were different for each species. The mechanics of capture by these species of diverse morphology and taxonomic affinity suggests that the use of bell pulsation-induced flow for prey entrainment and capture is widespread among the scyphomedusae.

Transitions of Mnemiopsis leidyi (Ctenophora: Lobata) from a native to an exotic species: a review

The genus Mnemiopsis is comprised of a single species, Mnemiopsis leidyi A. Agassiz, 1865, that has recently made the transition from a distribution limited to the Atlantic coasts of North and South America to an invasive range that includes the Black, Caspian, Mediterranean, North, and Baltic seas. We review the foundations of the ctenophore’s invasive success, which include the source-sink dynamics that characterize Mnemiopsis populations in temperate coastal waters where the ctenophore achieves its highest biomass levels and ecosystem impacts. Within its native temperate range, Mnemiopsis is frequently a dominant, seasonal, colonizing species with limited dispersal capacities. Cross-oceanic transport within ballast waters of intercontinental shipping vessels has altered this dispersal limitation and initiated a rapid global spread of Mnemiopsis. Owing to continuing transport via transoceanic shipping, we anticipate continued range expansion and review the variables most likely to determine whether introduction of Mnemiopsis to a novel community results in an inconspicuous addition or a disruptive invasion.

A wake-based correlate of swimming performance and foraging behavior in seven co-occurring jellyfish species.

SUMMARY It is generally accepted that animal–fluid interactions have shaped the evolution of animals that swim and fly. However, the functional ecological advantages associated with those adaptations are currently difficult to predict on the basis of measurements of the animal–fluid interactions. We report the identification of a robust, fluid dynamic correlate of distinct ecological functions in seven jellyfish species that represent a broad range of morphologies and foraging modes. Since the comparative study is based on properties of the vortex wake – specifically, a fluid dynamical concept called optimal vortex formation – and not on details of animal morphology or phylogeny, we propose that higher organisms can also be understood in terms of these fluid dynamic organizing principles. This enables a quantitative, physically based understanding of how alterations in the fluid dynamics of aquatic and aerial animals throughout their evolution can result in distinct ecological functions.

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

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

Passive energy recapture in jellyfish contributes to propulsive advantage over other metazoans

Significance Jellyfish have the ability to bloom and take over perturbed ecosystems, but this is counterintuitive because jellyfish are described as inefficient swimmers and rely on direct contact with prey to feed. To understand how jellyfish can outcompete effective visual hunters, such as fish, we investigate the energetics of propulsion. We find that jellyfish exhibit a unique mechanism of passive energy recapture, which can reduce metabolic energy demand by swimming muscles. Contrary to prevailing views, this contributes to jellyfish being one of the most energetically efficient propulsors on the planet. These results demonstrate a physical basis for the ecological success of medusan swimmers despite their simple body plan and have implications for bioinspired design, where low-energy propulsion is required. Gelatinous zooplankton populations are well known for their ability to take over perturbed ecosystems. The ability of these animals to outcompete and functionally replace fish that exhibit an effective visual predatory mode is counterintuitive because jellyfish are described as inefficient swimmers that must rely on direct contact with prey to feed. We show that jellyfish exhibit a unique mechanism of passive energy recapture, which is exploited to allow them to travel 30% further each swimming cycle, thereby reducing metabolic energy demand by swimming muscles. By accounting for large interspecific differences in net metabolic rates, we demonstrate, contrary to prevailing views, that the jellyfish (Aurelia aurita) is one of the most energetically efficient propulsors on the planet, exhibiting a cost of transport (joules per kilogram per meter) lower than other metazoans. We estimate that reduced metabolic demand by passive energy recapture improves the cost of transport by 48%, allowing jellyfish to achieve the large sizes required for sufficient prey encounters. Pressure calculations, using both computational fluid dynamics and a newly developed method from empirical velocity field measurements, demonstrate that this extra thrust results from positive pressure created by a vortex ring underneath the bell during the refilling phase of swimming. These results demonstrate a physical basis for the ecological success of medusan swimmers despite their simple body plan. Results from this study also have implications for bioinspired design, where low-energy propulsion is required.

An algorithm to estimate unsteady and quasi-steady pressure fields from velocity field measurements

We describe and characterize a method for estimating the pressure field corresponding to velocity field measurements such as those obtained by using particle image velocimetry. The pressure gradient is estimated from a time series of velocity fields for unsteady calculations or from a single velocity field for quasi-steady calculations. The corresponding pressure field is determined based on median polling of several integration paths through the pressure gradient field in order to reduce the effect of measurement errors that accumulate along individual integration paths. Integration paths are restricted to the nodes of the measured velocity field, thereby eliminating the need for measurement interpolation during this step and significantly reducing the computational cost of the algorithm relative to previous approaches. The method is validated by using numerically simulated flow past a stationary, two-dimensional bluff body and a computational model of a three-dimensional, self-propelled anguilliform swimmer to study the effects of spatial and temporal resolution, domain size, signal-to-noise ratio and out-of-plane effects. Particle image velocimetry measurements of a freely swimming jellyfish medusa and a freely swimming lamprey are analyzed using the method to demonstrate the efficacy of the approach when applied to empirical data.

Bending rules for animal propulsion

Animal propulsors such as wings and fins bend during motion and these bending patterns are believed to contribute to the high efficiency of animal movements compared with those of man-made designs. However, efforts to implement flexible designs have been met with contradictory performance results. Consequently, there is no clear understanding of the role played by propulsor flexibility or, more fundamentally, how flexible propulsors should be designed for optimal performance. Here we demonstrate that during steady-state motion by a wide range of animals, from fruit flies to humpback whales, operating in either air or water, natural propulsors bend in similar ways within a highly predictable range of characteristic motions. By providing empirical design criteria derived from natural propulsors that have convergently arrived at a limited design space, these results provide a new framework from which to understand and design flexible propulsors.

Morphological diversity of medusan lineages constrained by animal-fluid interactions.

SUMMARY Cnidarian medusae, commonly known as jellyfish, represent the earliest known animal taxa to achieve locomotion using muscle power. Propulsion by medusae requires the force of bell contraction to generate forward thrust. However, thrust production is limited in medusae by the primitive structure of their epitheliomuscular cells. This paper demonstrates that constraints in available locomotor muscular force result in a trade-off between high-thrust swimming via jet propulsion and high-efficiency swimming via a combined jet-paddling propulsion. This trade-off is reflected in the morphological diversity of medusae, which exhibit a range of fineness ratios (i.e. the ratio between bell height and diameter) and small body size in the high-thrust regime, and low fineness ratios and large body size in the high-efficiency regime. A quantitative model of the animal–fluid interactions that dictate this trade-off is developed and validated by comparison with morphological data collected from 660 extant medusan species ranging in size from 300 μm to over 2 m. These results demonstrate a biomechanical basis linking fluid dynamics and the evolution of medusan bell morphology. We believe these to be the organising principles for muscle-driven motility in Cnidaria.