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

Brad J. Gemmell; John H. Costello; Sean P. Colin; Colin J. Stewart; John O. Dabiri; Danesh Tafti; Shashank Priya

doi:10.1073/pnas.1306983110

New Research In

Edited by Steven Vogel, Duke University, Durham, NC, and accepted by the Editorial Board August 21, 2013 (received for review April 16, 2013)

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.

Abstract

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.

Footnotes

↵¹To whom correspondence should be addressed. E-mail: bgemmell{at}mbl.edu.

Author contributions: B.J.G., J.H.C., and S.P.C. designed research; B.J.G. performed research; C.J.S., J.O.D., D.T., and S.P. contributed new reagents/analytic tools; B.J.G., C.J.S., and J.O.D. analyzed data; and B.J.G., J.H.C., S.P.C., and J.O.D. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission. S.V. is a guest editor invited by the Editorial Board.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1306983110/-/DCSupplemental.