A ctenophore (comb jelly) employs vortex rebound dynamics and outperforms other gelatinous swimmers

Abstract

Gelatinous zooplankton exhibit a wide range of propulsive swimming modes. One of the most energetically efficient is the rowing behaviour exhibited by many species of schyphomedusae, which employ vortex interactions to achieve this result. Ctenophores (comb jellies) typically use a slow swimming, cilia-based mode of propulsion. However, species within the genus Ocyropsis have developed an additional propulsive strategy of rowing the lobes, which are normally used for feeding, in order to rapidly escape from predators. In this study, we used high-speed digital particle image velocimetry to examine the kinematics and fluid dynamics of this rarely studied propulsive mechanism. This mechanism allows Ocyropsis to achieve size-adjusted speeds that are nearly double those of other large gelatinous swimmers. The investigation of the fluid dynamic basis of this escape mode reveals novel vortex interactions that have not previously been described for other biological propulsion systems. The arrangement of vortices during escape swimming produces a similar configuration and impact as that of the well-studied 'vortex rebound' phenomenon which occurs when a vortex ring approaches a solid wall. These results extend our understanding of how animals use vortex-vortex interactions and provide important insights that can inform the bioinspired engineering of propulsion systems.

Keywords: bioengineering; biomechanics; jellyfish; plankton; propulsion; vortex interactions.

Figure 1.

Swimming performance metrics. (a) Change in body fineness over time for a representative escape swimming sequence in the ctenophore O. maculata. (b) Instantaneous velocity over the escape sequence. (c) Instantaneous acceleration over the escape sequence. (d) Maximum attained swimming speeds in terms of body lengths per second for O. maculata and six other large (greater than 2 cm) gelatinous swimmers. Light grey bars, ctenophores; black bars, scyphomedusae; white bars, cubomedusae; dark grey bar, salp. Data for other gelatinous swimmers from: [,,–17]. Ocyropsis maculata uses fast swimming only in short bursts, while other species listed tend to be continuous swimmers.

Figure 2.

Lobe kinematics of O. maculata in comparison to the rowing medusa A. aurita. (a) Sequential images of O. maculata at different times during its swimming cycle. The cycle starts with lobe expansion (images 1–3) and finishes with a very rapid contraction (images 3–5). (b) An outline of the outer edge of the lobe shows the relative position of the O. maculata lobe (normalized to the apex) throughout the expansion and contraction phases. The bell outline (in red) of the scyphomedusae A. aurita underlays the O. maculata outline to illustrate the differences between O. maculata kinematics and that of a typical rowing medusae. The inset (c) shows the velocity of the tip of the lobe throughout the swim cycle. In essence, the lobe of O. maculata moves much faster (inset c) and over a much longer distance than typical rowing medusae.

Figure 3.

Fluid mechanics (velocity vectors and vorticity contours) from two gelatinous swimmers that employ rowing-based kinematics. (a–d) The ctenophore O. maculata. Note that the stopping vortex (indicated by yellow arrows) forms underneath the body during the expansion phase (b) but continues to move outside the lobes such that when the contraction begins, the stopping vortex is located outside of the newly formed starting vortex (c). The result of the vortex–vortex interaction is no net movement of the vortex superstructure (d). (e–h) The moon jellyfish A. aurita. Here, the stopping vortex (indicated by yellow arrows) remains confined under the jellyfish bell (e–g). The result is the downward movement of the entire vortex superstructure (h).

Figure 4.

Fluid mechanics (velocity vectors and vorticity contours) of one side of the vortex superstructure shed by O. maculata. Note that while the animal moved its lobes and the resulting starting vortex in a downward direction, the starting vortex (red) is simultaneously pulled upwards (as indicated by yellow arrows) due to interaction with the opposite sign stopping vortex (blue). The result is a vertically elongated vortex superstructure.

Figure 5.

Conceptual figure illustrating a proposed mechanism for enhancing biological propulsion through the arrangement of vortices into a ‘vortex rebound’ configuration. (a) Vortex–vortex interactions cause a rebound effect, which pulls the entire vortex superstructure upwards (difference between the dotted lines). Based on data from Orlandi [29]. (b) Vortex configuration observed during escape swimming in the ctenophore O. maculata. Note that instead of the vortex superstructure being pulled upwards, the starting (inner) vortex is stretched as the animal pushes downwards with its lobes. This could result in greater overall thrust for the animal. (c) A hypothetical case based on medusae rowing-type swimming where the starting vortex is ejected backwards into the wake. Here, the reaction force on the lobes would be lower than that in (b) and would lead to lower thrust. Black arrows show net motion of vortex superstructure; green arrows show net thrust of ctenophore.