Passive Energy Recapture in Jellyfish Contributes to Propulsive Advantage over other Metazoans

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

Prey capture by the cosmopolitan hydromedusae, Obelia spp., in the viscous regime

Author Posting. © Association for the Sciences of Limnology and Oceanography, 2016. This article is posted here by permission of Association for the Sciences of Limnology and Oceanography for personal use, not for redistribution. The definitive version was published in Limnology and Oceanography 61 (2016): 2309–2317, doi:10.1002/lno.10390.Obelia spp. are cnidarian hydromedusae with a cosmopolitan distribution but very little is known about their feeding. The small size of Obelia (bell diameter ∼ 1 mm, tentacle width ∼ 0.05 mm) suggests that feeding occurs in a viscous regime characterized by thick boundary layers. During feeding observations with a natural prey assemblage the majority of prey were captured at the tentacle tips during the contraction phase. Swimming kinematics from high speed videography confirmed that swimming was a low Re number process (Re < 50) and showed that maximum tentacle velocities occurred at the tentacle tips midway through a bell contraction. Flow visualizations from particle image velocimetry demonstrated that fluid motion between the tentacles was limited and that velocities were highest at the tentacle tips, leading to a thinning of boundary layer in this region. The highest nematocyst densities were observed in this same region of the tentacle tips. Taken together, the body kinematics, flow visualizations and nematocyst distributions of Obelia explain how these predators are able to shed viscous boundary layers to effectively capture microplanktonic prey. Our findings help explain how other small feeding-current medusae whose feeding interactions are governed by viscosity are able to successfully forage.National Science Foundation Grant Numbers: OCE- 1155084, DBI- 1455471, OCE- 1536672, OCE- 153668

Maneuvering performance in the colonial siphonophore, Nanomia bijuga

© The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Sutherland, K. R., Gemmell, B. J., Colin, S. P., & Costello, J. H. Maneuvering performance in the colonial siphonophore, Nanomia bijuga. Biomimetics, 4(3), (2019): 62, doi:10.3390/biomimetics4030062.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.This research was funded by the National Science Foundation (NSF) 1829932 and 173764 to K.R.S., NSF 1830015, 1536672, 1511721 to J.H.C., 1455440, 1536688, 1829913 to S.P.C., NSF 1511996 to B.J.G

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

Ink release and swimming behavior in the oceanic Ctenophore Eurhamphaea vexilligera

Author Posting. © University of Chicago, 2020. This article is posted here by permission of University of Chicago for personal use, not for redistribution. The definitive version was published in Biological Bulletin 238(3), (2020): 206-213. doi:10.1086/709504.Of the more than 150 ctenophore species, the oceanic ctenophore Eurhamphaea vexilligera is notable for its bright orange-yellow ink, secreted from numerous small vesicles that line its substomodeal comb rows. To date, in situ observations by scuba divers have proved the most fruitful method of observing these animals’ natural behavior. We present the results of one such contemporary scuba-based observation of E. vexilligera, conducted in the Gulf Stream waters off the coast of Florida, using high-resolution photography and video. Utilizing underwater camera systems purpose built for filming gelatinous zooplankton, we observed E. vexilligera ink release and swimming behavior in situ. From these data, we describe the timeline and mechanics of E. vexilligera ink release in detail, as well as the animal’s different swimming behaviors and resulting ink dispersal patterns. We also describe a rolling swimming behavior, accompanied and possibly facilitated by a characteristic change in overall body shape. These observations provide further insight into the behavioral ecology of this distinctive ctenophore and may serve as the foundation for future kinematic studies.This work was funded by National Science Foundation awards OCE-1829945 to BJG, OCE-1829932 to KRS, OCE-1829913 to SPC, and OCE-1830015 to JHC. We thank the captain and crew of Calypso Dive Charters’ Miss Jackie for their assistance and field expertise, as well as two anonymous reviewers, whose insightful comments have improved the quality of the manuscript

Jellyfish and Fish Solve the Challenges of Turning Dynamics Similarly to Achieve High Maneuverability

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

Field testing of biohybrid robotic jellyfish to demonstrate enhanced swimming speeds

© The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Xu, N. W., Townsend, J. P., Costello, J. H., Colin, S. P., Gemmell, B. J., & Dabiri, J. O. Field testing of biohybrid robotic jellyfish to demonstrate enhanced swimming speeds. Biomimetics, 5(4), (2020): E64, doi:10.3390/biomimetics5040064.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.This work was supported by the National Science Foundation (NSF) Graduate Research Fellowship Program (GRFP) awarded to N.W.X

Biomimetic and Live Medusae Reveal the Mechanistic Advantages of a Flexible Bell Margin

Flexible bell margins are characteristic components of rowing medusan morphologies and are expected to contribute towards their high propulsive efficiency. However, the mechanistic basis of thrust augmentation by flexible propulsors remained unresolved, so the impact of bell margin flexibility on medusan swimming has also remained unresolved. We used biomimetic robotic jellyfish vehicles to elucidate that propulsive thrust enhancement by flexible medusan bell margins relies upon fluid dynamic interactions between entrained flows at the inflexion point of the exumbrella and flows expelled from under the bell. Coalescence of flows from these two regions resulted in enhanced fluid circulation and, therefore, thrust augmentation for flexible margins of both medusan vehicles and living medusae. Using particle image velocimetry (PIV) data we estimated pressure fields to demonstrate a mechanistic basis of enhanced flows associated with the flexible bell margin. Performance of vehicles with flexible margins was further enhanced by vortex interactions that occur during bell expansion. Hydrodynamic and performance similarities between robotic vehicles and live animals demonstrated that the propulsive advantages of flexible margins found in nature can be emulated by human-engineered propulsors. Although medusae are simple animal models for description of this process, these results may contribute towards understanding the performance of flexible margins among other animal lineages

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

© The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Colin, S. P., Costello, J. H., Sutherland, K. R., Gemmell, B. J., Dabiri, J. O., & Du Clos, K. T. The role of suction thrust in the metachronal paddles of swimming invertebrates. Scientific Reports, 10(1), (2020): 17790, doi:10.1038/s41598-020-74745-y.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.This work was funded by National Science Foundation (NSF OCE 1829913 to SPC), the Alfred P. Sloan Foundation (to BJG) and the Gordon and Betty Moore Foundation (8835 to KRS). The work was also supported by the Roger Williams Foundation to Promote Scholarship and Teaching

Resilience in moving water : effects of turbulence on the predatory impact of the lobate ctenophore Mnemiopsis leidyi

© The Author(s), 2017. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Limnology and Oceanography 63 (2018): 445–458, doi:10.1002/lno.10642.Despite its delicate morphology, the lobate ctenophore Mnemiopsis leidyi thrives in coastal ecosystems as an influential zooplankton predator. Coastal ecosystems are often characterized as energetic systems with high levels of natural turbulence in the water column. To understand how natural wind-driven turbulence affects the feeding ecology of M. leidyi, we used a combination of approaches to quantify how naturally and laboratory generated turbulence affects the behavior, feeding processes and feeding impact of M. leidyi. Experiments using laboratory generated turbulence demonstrated that turbulence can reduce M. leidyi feeding rates on copepods and Artemia nauplii by > 50%. However, detailed feeding data from the field, collected during highly variable surface conditions, showed that wind-driven turbulence did not affect the feeding rates or prey selection of M. leidyi. Additional laboratory experiments and field observations suggest that the feeding process of M. leidyi is resilient to wind-driven turbulence because M. leidyi shows a behavioral response to turbulence by moving deeper in the water column. Seeking refuge in deeper waters enables M. leidyi to maintain high feeding rates even under high turbulence conditions generated by wind driven mixing. As a result, M. leidyi exerted a consistently high predatory impact on prey populations during highly variable and often energetic wind-driven mixing conditions. This resilience adds to our understanding of how M. leidyi can thrive in a wide spectrum of environments around the world. The limits to this resilience also set boundaries to its range expansion into novel areas.Seventh Framework Programme Grant Number: 600207; Division of Ocean Sciences Grant Number: 106118