1. Lecture 8, Bio 325 Jetting locomotion by prolate and oblate medusae Squid locomotion Assigned reading: Dabiri J. O., Colin S.P., Costello J.H., Gharib, M. 2005. Flow patterns generated by oblate medusan jellyfish: field measurements and laboratory analyses. Journal of experimental Biology 208: 1257- in which they discover the stopping vortex ring which contributes to medusa swimming. JELLYFISH FORM AND FUNCTION Website by John H. Costello & Sean P. Colin, Roger Williams University. See this website for information about jellyfish swimming: fox.rwu.edu/jellies/index.html Gemmell B.J. et al. 2013. Passive energy recapture in jellyfish contributes to propulsive advantage over other metazoans. PNAS 110: 17904- Gosline J.M., & Demont M.E. 1984. Jet-propelled swimming in squids. Scientific American 252: 96-103.

2. Vortices When I draw a canoe paddle through still water on a lake, I see small vortices trail off the paddle edges downflow. When I stir coffee or let water down the drain I make vortices. Smokers blow smoke rings and cetaceans blow bubble rings. This picture is of a vortex forming on the upstream side of a tidal turbine*. These rings travel through the fluid. Fluids like water and air exhibit flow and a vortex is simply flow that spins. Toroid: doughnut-shaped object, e.g., O ring toroidal vortices produced behind swimming jellyfish *the ‘hole’ in the centre is ~15 cm in diameter songofthepaddle

3. Cnidarian morphs: Polyps (e.g., sea anemones) and Medusae (e.g., Jellyfish) -In contrast to the polypoid mesoglea (middle layer), which is more or less thin, the medusoid mesoglea is extremely thick and constitutes the bulk of the animal.” (from Barnes) What is the function of mesoglea in a jellyfish? Buoyancy? Antagonist? Why is the mesoglea of the locomotory morph so much more important (based on its abundance) than the mesoglea of the sessile morph? Mesoglea another body material: a pliant composite material The mesoglea of jellyfish is adapted as a viscoelastic antagonist of the bell’s circular muscles.

4. Medusae can be bullet-shaped (prolate) or flatter (oblate) Velum has to do with shaping vortices Oblate medusae have smaller velums than prolate, contract more slowly when swimming and throw larger amounts of water behind them as they jet. prolate oblate

5. Jet propulsion and vortices Animal Literature More complex: Dabiri et al. : jellyfish jetts out seawater making 2 vortex rings --“doughnuts of water that are continuously rolling into themselves”. oblate medusaBarnes: Simplest swimming explanation: seawater beneath the umbrella is incompressible; coronal muscle, powerful circular fibres on the subumbrella contracts to jet out the subumbrellar fluid.

6. Jetting by Jellyfish

7. Schematic of a jetting medusa with vortex rings in the wake. Dabiri J O et al. J Exp Biol 2005;208:1257-1265 ©2005 by The Company of Biologists Ltd Jetting medusa with vortex rings in wake Periodic bell contractions decrease volume of subumbrellar cavity, displacing out the high bulk modulus (incompressible) water as a jet: jet propulsion. Swimming cycle: fluid efflux emerges during bell contraction: a toroidal volume of rotating fluid known as the power stroke starting vortex ring. This travels downstream – is shed -- behind the forward progress of the medusa. There are two things in the wake: this vortex and a central jet (D). The cycle continues with a second fluid efflux shed during bell relaxation and recovery, a recovery stroke stopping vortex ring as mesoglea returns its elastic force. of distortion, elastic force)

8. Kinematics of the starting, stopping and co-joined lateral vortex structures. Dabiri J O et al. J Exp Biol 2005;208:1257-1265 ©2005 by The Company of Biologists Ltd Dye used to visualize the behaviour of the fluid in the wake of the swimming medusa. Starting vortex ring involves fluid originating from ‘regions inside the subumbrellar volume’, but also from outside the bell via ‘entrainment of ambient fluid’ [flow induced by vortex rotation]; motion of this ring is oriented at an angle away from the bell margin toward the central axis of the bell and downstream (broken arrows). ambient: surrounding solid arrows: direction of vortex rotation

9. Kinematics of the starting, stopping and co-joined lateral vortex structures. Stopping vortex ring: bell coronal muscle fibres relax and bell opens (mesoglea returns energy for this that originated with the coronal muscle). This bell recoil makes a stopping vortex initially within the subumbrellar cavity. But fluid originating from outside the bell is also entrained: it is drawn toward the subumbrellar cavity.”

10. My first attempt to make these ‘kinematics’ comprehensible to make the information my own. Drawings, scribbles are important to me in this process. I recommend something like this for both learning and for testing. L1/L2, adjacent lateral vortex superstructures created between the two toroids. Stopping vortex lateral structure contributes to advance of swimmer during recovery cycle.

11. Gemmell B.J. et al. 2013. Passive energy recapture in jellyfish contributes to propulsive advantage over other metazoans. PNAS 110: 17904- “Gelatinous zooplankton” (jellyfish) blooms are problems in ‘perturbed ecosystems’. How are jellyfish able to do so much better than the fish? Jellyfish are such apparently poor swimmers, so ‘primitive’ and inefficient in comparison to fish; how can they so thoroughly outcompete fish in these degraded habitats? Note that both medusae and fish have to pursue their food in the water column, i.e., swim after what they eat rather than filter it out of currents bringing food to them: we are comparing animal predators that pursue their food and must “rely on direct contact with prey to feed”. The ‘passive energy recapture’ involved in the vortices is credited with this greater locomotion efficiency: [from abstract of Gemmell] “...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.” Jellyfish are “one of the most energetically efficient propulsors on the planet”.

12. Nature News, October 2013, Ed Yong: “The sockeye salmon is a sleek torpedo that uses its strong muscles to leap up waterfalls. The moon jellyfish (Aurelia aurita) is a flimsy blob that drifts along like a gently pulsating bell. The salmon is obviously the more powerful swimmer, but a study has revealed that the jellyfish outclasses it in efficiency. For its mass the jellyfish spends less energy to travel a given distance than any other swimming animal.” “When moon jellyfish contract their umbrella-shaped bells, they create two vortex rings – doughnuts of water that are continuously rolling into themselves. The creature sheds the first ring in its wake, propelling itself forward. As the bell relaxes, the second vortex ring rolls under it and starts to spin faster. This sucks in water which pushes up against the centre of the jellyfish and gives it a secondary boost...” Maybe explanation of role of stopping vortices in jellyfish locomotion is easier to understand in Gemmel (and Yong)?

13. Phylum Mollusca Shell is a skeleton that doesn’t function in locomotion. Snail body, visceral mass and foot, seems amorphous; these animals are ‘shape-shifters’ (octopus reknowned for escaping cages through cracks): versatility in body shape change marks the importance of its hydraulic skeleton: its use of fluid force translocation in moving about: changing body shape by the interaction of fluid and muscle and collagen fibres Land snail

14. A mollusc ancestral to squids, to see how foot shell & mantle cavity changed during evolution

15. streamlining dorsal view Shell is an internal remnant sunk within the mantle tissue; it is called the pen

16. Funnel (not visible in this photo) developed from posterior of primitive foot. Primitive ventral surface of ancestor became functional anterior end. Chromatophores are pigment cells in skin, circlet of smooth muscle cells, disperse concentrate. Class Cephalopoda includes squid, octopus, cuttlefish, Nautilus primitive dorsum Fins set up waves; posterior lateral fins act as stabilizers and rudders; squids achieve greatest swimming speeds of any aquatic invertebrate, up to 40 kmph.

17. Assigned reading: Gosline J.M., & Demont M.E. 1984. Jet-propelled swimming in squids. Scientific American 252: 96-103. A swimming squid takes up and expels water by contracting radial and circular muscles in its boneless mantle wall. Elastic collagen “springs” in the muscle increase the power of the jet. Beware potential confusion: squids jet-propel themselves and of course there is a fluid-filled cavity involved – the mantle cavity. The seawater in this cavity functions in locomotion by virtue of its high bulk modulus; if the seawater were not incompressible the jetting wouldn’t work. But this cavity is NOT functioning as a hydrostatic skeleton antagonizing mantle muscles. Rather the mantle wall itself is a muscular hydrostat.

18. The seawater within the mantle cavity of the squid is not functioning as a hydrostatic skeleton. But it is the basis of the animal's jet propulsion, which in turn depends upon the incompressibility of seawater. When the radial muscles of the mantle contract, the volume of the mantle cavity is increased and seawater is drawn in. When the circular muscles of the mantle contract, the volume of the mantle cavity is decreased and seawater is squirted out. The action-force of the jetted seawater creates a reaction force that pushes the squid in the opposite direction: opposite to whatever direction the funnel is pointing. One-way valves* control intake of water into mantle cavity at sides. Pressure build up in seawater inside mantle cavity (circulars contract) forces the inner flaps of the funnel against the mantle wall water jets out funnel (hypostome). [*recall starfish canals]

19. In the mantle structures interact: 1) collagen fibres make a tunic that prevents longitudinal dimension change 2) radial muscles contract to thin the mantle wall and 3) circular muscles of the mantle contract to thicken the wall. Circulars and radials are antagonists. The mantle (the actual wall) is a muscular hydrostat and its volume must stay constant (just as if it were a fluid-filled cavity). But (per Kier) the fibres are very critical: because of the collagen ‘tunic’ the mantle cannot get longer in the A to B dimension: it can change in girth. [Imagine as it isn’t: no tunic: would lengthen in response to circulars.] A B

20. 1.Radial muscles contract to cause: hyperinflation: seawater intake into mantle cavity: outside diameter of mantle increases by approximately 10% over resting diameter (girth increase); cavity volume increases 22% re relaxed volume, wall thins. 2. Circular muscles contract to bring mantle to about 75% of its relaxed diameter, radials restored to precontracted length (girth decrease): volume drops & pressure rises sharply, forcing the inlet valvesl against the mantle wall and leaving only the funnel as exit. relaxed Mantle wall Escape Jet Cycle of squid Internal organs contracted

21. The mantle wall functions as a muscular hydrostat -- a fluid-based skeleton [muscles mostly water] without a distinct fluid chamber -- it makes antagonists of the radial and circular muscles: contraction of one kind of muscle restores the other to its relaxed state via this type of fluid skeleton. The radial and circular muscles become coupled as antagonists by virtue of their own tissue being significantly water and so incompressible – and because the mantle cannot lengthen. Because the mantle is incompressible it must retain an overall constant volume; and it cannot get longer as mantle muscles contract because of the collagen fibre tunic that prevents any movement in that direction. Thus, it can only increase or decrease in thickness – at the same time changing its overall diameter and the capacity of the mantle cavity. When the radials contract the mantle walls must get thinner and the walls move apart -- to maintain hydrostat volume. Conversely when the circulars contract the mantle wall must get thicker as the overall outside diameter of the mantle decreases. If there were no inextensible fibres, if the animal’s mantle was not in a jacket of fibres preventing it from lengthening, then the radials and the circulars could not have an antagonistic effect on each other.