Phenotypic plasticity in juvenile jellyfish medusae facilitates effective animal-fluid interaction

Abstract

Locomotion and feeding in marine animals are intimately linked to the flow dynamics created by specialized body parts. This interaction is of particular importance during ontogeny, when changes in behaviour and scale challenge the organism with shifts in fluid regimes and altered functionality. Previous studies have indicated that Scyphozoan jellyfish ontogeny accommodates the changes in fluid dynamics associated with increasing body dimensions and velocities during development. However, in addition to scale and behaviour that-to a certain degree-underlie the control of the animal, flow dynamics are also dependent on external factors such as temperature. Here, we show phenotypic plasticity in juvenile Aurelia aurita medusae, where morphogenesis is adapted to altered fluid regimes imposed by changes in ambient temperature. In particular, differential proportional growth was found to compensate for temperature-dependent changes in viscous effects, enabling the animal to use adhering water boundary layers as 'paddles'-and thus economize tissue-at low temperatures, while switching to tissue-dominated propulsion at higher temperatures where the boundary layer thickness is insufficient to serve for paddling. This effect was predicted by a model of animal-fluid interaction and confirmed empirically by flow-field visualization and assays of propulsion efficiency.

Figure 1.

(a) Characteristic parameters of ephyra morphology. A, potential bell area; D, diameter; r, radial lappet position; b(r), lappet width at radial position r. (b) Model of boundary layer formation on solid surface. U, velocity. Arrows represent velocities relative to free stream flow. Thickness of boundary layer (δ) denotes distance from solid surface to the point where U_fluid = 0.99 × U_{free stream}. (c) Schematic illustration of the two operation modes of the lappet array with different flow Reynolds numbers: (i) filter mode with no boundary layer overlap (high Re); (ii) paddle mode with complete boundary layer overlap (low Re). Different shades of blue correspond to velocity gradient in boundary layer as in (b). (d) Stokes model of bell continuity (BC) as a function of diameter, with C = 0.8. Blue line, model for 13°C; black dashed line, model for 21°C. (e) Morphometric data of Aurelia aurita. BC is plotted against diameter. Blue circles, G₁₃ ephyrae; white circles, G₂₁ ephyrae. Right: two ephyrae from G₂₁ (top) and G₁₃ (bottom) are depicted to illustrate the differences in morphology. (f) Histogram of BC values of the two temperature groups (n = 41 for each group, equal distribution of diameters). Blue bars, G₁₃ ephyrae; black striped bars, G₂₁ ephyrae. (g) Model of continuous boundary layer overlap at all stages of bell development.

Figure 2.

Dye visualization of boundary layer during powerstroke. Dotted line indicates outline of animal body. BL, boundary layer. (a) Sieve-mode: G₁₃ ephyra swimming at 21°C water temperature. (i) Start of powerstroke, bell is fully relaxed, (ii) end of powerstroke, bell is fully contracted. Note that the thin boundary layer outlines the body but fails to connect between lappets. (b) Paddle-mode: G₁₃ ephyra swimming at 13°C water temperature. (i) Start of powerstroke, bell is fully relaxed, (ii) end of powerstroke, bell is fully contracted. Note the delay in boundary layer motion when compared with body motion, visualizing the velocity gradient at the fluid–solid interface. (c) Parameters of ephyra propulsion. r, Radial position along lappet; θ, swept angle; ω, angular velocity; L_B, body length. (d) Effect of ambient water temperature on propulsion efficiency of G₁₃ ephyrae. Box plots show body length travelled per stroke at 13°C (n = 7) and at 21°C (n = 7). White marks correspond to median, the edges of the box are 25th and 75th percentiles, whiskers indicate extreme data points not considered outliers. Outliers are plotted as individual squares. Asterisk represents significant difference in median values.