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

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.

Keywords: animal-fluid interactions; swimming efficiency.

Fig. 1.

Energetic swimming comparisons of propulsive modes. (A) Net COT based on wet mass. Data for fliers and runners are replotted from the study by Schmidt-Nielsen (30). Crustaceans and squid are replotted from the study by Larson (12). Fish data were combined from both of these studies (12, 30). Data for A. aurita were calculated with swimming speed vs. body size from the current study and supplemented with data from the studies by Martin (27) and McHenry and Jed (28) and by metabolic data from the study by Uye and Shimauchi (29). (B) Net respiration rates of locomotion for the salmon (O. nerka) and a rhizostome jellyfish (S. meleagris). (C) Net respiration rates of locomotion for S. meleagris and A. aurita. (D) Net COT for all three species. Data used for respiration and COT in salmon were obtained from the study by Brett and Glass (31), and Stomolophus data were replotted from the study by Larson (32). WW, wet weight.

Fig. 2.

Swimming performance of A. aurita. (A) Maximum circulation and vorticity starting and stopping vortices during normal swimming (cruising). (Scale bar, 1 cm.) (B) Representative swimming sequence of a 3-cm A. aurita, showing an increase in speed during periods of no kinematic body motion (postrecovery). The model (red) shows a conservative estimate of the change in speed with time from inertia alone. (C) Cumulative distance of the jellyfish shown in B. Yellow represents the distance gained from passive energy recapture. (D) Effect of passive energy recapture with size (bell diameter). No difference (P = 0.550) is observed between body size and the relationship between distance traveled from passive energy recapture (D_PR) relative to the total distance traveled per swimming stroke (D_Tot).

Fig. 3.

Swimming performance for three species of jellyfish showing species variation in the durations of contraction (I), relaxation/refilling (II), and the interpulse duration during which thrust from passive energy recapture occurs (III). All three species exhibit enhanced thrust during this third phase. (A) Oblate scyphomedusae, A. aurita. (B) Hydromedusae, Eutonina indicans. (C) Rhizostome, Phyllorhiza punctata. (D) Cumulative swimming distance for all three species.

Fig. 4.

CFD of a 3-cm swimming A. aurita. (A) Pressure around the body during a swimming cycle. Note the secondary increase in pressure at the subumbrellar surface (VI–VIII) and the resulting axial force and boost in velocity. (B) Axial force shows the corresponding locations from A. A secondary peak is shown corresponding to positive pressure of the induced flow created by the stopping vortex accumulating against the subumbrellar surface. (C) Velocity-time plot shows the corresponding locations from A. (D) Results from an empirically based technique for pressure estimation from velocity field measurements around a 3.5-cm A. aurita. (E) Velocity-time plot shows the corresponding locations from D.