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Jet Propulsion and the Evolution of the Cephalopods BULLETIN OF MARINE SCIENCE, 49(1-2): 419-432, 1991 JET PROPULSION AND THE EVOLUTION OF THE CEPHALOPODS M. J. Wells and R. K. O'Dor ABSTRACT The first cephalopods, recognized as such by their possession of a chambered shell with a siphuncle, appeared in the late Cambrian. They are assumed to have been crawling animals. Lightening the shell, made possible by ion and water removal and the consequent appearance of gas in the chambers would have allowed the animal to escape upwards, using the jet resulting from a sudden withdrawal of the body into the shell. Nautilus still produces a propulsive jet in this manner. It can also generate a low pressure stream using the wings of the funnel to waft a flow through the gills. It is argued that all the other ectocochleates would have had propulsive mechanisms based on one or other (or both) of the means by which Nautilus develops ajet. One consequence of this conclusion is that none of them were powerful swimmers. The momentum imparted by a jet depends upon the ejected mass multiplied by the velocity of the jet. But E = lhmv' so that while slow speed propulsion using the ventilation stream can result in a very low cost of transport any attempt to achieve high speeds is very costly. Only marginal improvements could be made by lightening or streamlining the shell. More economical fast locomotion could only be achieved by increasing the volume of the mantle cavity, and this meant scrapping or internalizing the shell. It also necessitated the development ofa new set of propulsive muscles, in the wall of the mantle. Mantle musculature now took on both locomotor and ventilatory functions. The two functions have incompatible requirements; for efficient jet propulsion the stream volume should be maximized, while efficient oxygen uptake should minimize the flow. Octopods have optimized oxygen extrac- tion, the squids, in general are specialized for jet propulsion. In the teuthoids and octopods progressive shell reduction also led to the loss of neutral buoyancy, regained in some forms by ion-substitution in the tissues and an associated return to relatively slow-moving lifestyles. Jet propulsion remained an extravagant form of propulsion at all but the slowest speeds. Many coleoids, as a result, have moved on to develop yet another locomotor system, replacing jet propulsion by undulant fins. The one fact that everybody seems to know about cephalopods is that they are jet-propelled. What is less universally recognized is that many have additional means of moving, swimming by the use of fins or crawling on their arms, so that jet propulsion often constitutes a secondary rather than their primary means of locomotion. It is also often forgotten that the early shelled cephalopods used two quite different means of generating the jet, neither of which is found in the modern coleoids. This paper is a brief survey of the likely history ofjet propulsion in cephalopods, concentrating particularly on the state of affairs in the many forms with external shells, now almost universally extinct. From what we now know of the living Nautilus, it is possible to reconstruct the likely swimming performance of am- monoids and nautiloids, and to understand why the shelled forms were progres- sively replaced as sea conditions changed to favor the faster-moving coleoids. The Earliest Cephalopods. - The earliest mollusc unequivocally recognizable as a cephalopod is the late Cambrian Plectronoceras. The animal, believed to be de- rived from tall, endogastric monoplacophores, had septa and a siphuncle (Yoch- elson et al., 1973; Webers and Yochelson, 1989). The chambers could have been fluid or gas filled; the body in the final chamber was attached by muscles that would have pulled an assumed head and foot back into safety when danger threat- ened. Since the animal was largely enclosed in a shell, it must have had gills to 419 420 BULLETIN OF MARINE SCIENCE, VOL. 49, NO. 1-2,1991 increase the respiratory area and a pumped circulatory system. Gills are, in their nature, vulnerable, so it is reasonable to assume that Plectronoceras also had a mantle cavity. A sudden withdrawal of the head and body into the protection of the shell (the traditional medieval defense of molluscs) would have displaced fluid from the mantle cavity. This, one must suppose, was the origin of the jet; Nautilus. as we shall see, still produces a jet in this manner. The sudden backward thrust would itself have constituted a means of escape and any lightening of the shell would have improved the performance (dilution and gas production are linked, since withdrawal of salts sets up an osmotic gradient; water follows, dropping the pres- sure in the chambe:rs, causing gas to come out of solution in the blood-Denton and Gilpin-Brown, 1966). Neutral buoyancy, a further development of the ten- dency to lighten the: shell, freed the foot from its locomotor functions and allowed it, on the one hand, to extend as flaps that could be overlapped to form a jet- directing funnel, and, together with the head, to extend as a series of grasping tentacles. The early cephalopods presumably had beaks and a radula, since all their descendants did SO; they could have been scavengers, but they were also well suited to a predatory existence, dropping from above on the bottom-living fauna below. Straight Nautiloids. - The resulting animals did well, and the rapid evolution of a whole range of curved and straight nautiloids, some of massive size, was un- stoppable (Teichert, 1967). For a long time these animals dominated the marine mid-water (or, perhaps more accurately nekto-benthic) environment, cruising at will above the seafloor where their prey and potential competitors were still in the main defeated by gravity. Sharks did not appear until the Devonian, almost 100 million years later. A long straight or slightly coiled shell is a difficult thing to maneuver, even given a funnel capable of directing the jet. It cannot readily be propelled backwards, because it will slew to one side; a rocket can correct for this, but it is difficult to envisage an effective system based on a pulsed jet. The alternative of spinning the shell along its longitudinal axis is plainly absurd. The limited evidence that we have suggests that all but the earliest, ellesmer- oceratid, straight nautiloids moved with their shells horizontal. The first formed chambers typically show additional mineral deposits, assumed to be counter- weights laid down as the animal grew. Because of the difficulty of steering, straight nautiloids probably swam head first, with the jet directed backwards, under the animal, as Nautilus can do today (Fig. I). Tracks in Ordovician rocks terminating in orthocone shells (Orthonybyoceras) show that animals grounding to die came in blunt end first (Flower, 1955; other trace fossils, interpreted as tentacle marks in the same work are now believed to be worm tubes, see Osgood, 1970) Jet Propulsion in Nautilus. -Coiled nautiloids appeared in the early Ordovician. This modification of the design has a number of advantages. It keeps the center of buoyancy above the center of gravity, so there is no need to weight the apex of the shell. Even the modem, coiled Nautilus uses something like 80% of its buoyancy to support the shell (Denton and Gilpin-Brown, 1966), and any further addition of weight reduces the buoyancy available to support body flesh. Coiling, moreover, economizes in shell materials, since each whorl builds on the one before and mineral ballasting is unnecessary. And it makes the animal much more ma- neuverable, both forwards and backwards. The six living species of Nautilus all conform to this pattern. They are totally dependent upon the jet for propulsion. Since the shell form so closely resembles that of some Palaeozoic ectocochleates, WELLS AND O'DOR: EVOLUTION OF JET PROPULSION 421 Head RETRACTOR MUSCLE ATTACHMENT Figure I, Two means of producing a jet in Nautilus: 1) The very large paired head retractor muscles can pull down the head, expelling all water from the mantle cavity. 2) The wings of the funnel folds, hanging down from above and overlapping below, contract rhythmically to waft a steady flow of water (arrows) down through the gills and out through the funnel. The contents of the mantle cavity are shown a) from the right side and b) from below, Inset c) shows how the very flexible funnel can move to direct the jet to the side or backwards. (c) After Packard et al. (1980), it seems reasonable to conclude that Nautilus develops the jet in the same manner as did its ancestors. In fact, it generates the jet in two distinct ways. One of these reflects the ancestral escape mechanism; the head is drawn down into the shell aperture by the massive head retractor muscles, displacing water from the mantle cavity. The funnel is formed from two folds of muscle, hanging down from either side of the head, overlapping to form a highly maneuverable spout (Fig. 1). From the roof of the funnel hangs a flap-valve, so that water is not readily drawn back in by this route. Instead, re-extension of the head, caused by the active contraction of radial fibers in the head retractor muscles, plus, no doubt, by some elasticity in the rubbery head shield, sucks in water close to the umbilicus on either side; rearward exten- sions of the funnel folds here form further one-way valves. The second jet-producing system is the funnel itself. The very large funnel folds extend back along the whole length of the mantle cavity on either side. In quiet ventilation, these "wings" of the funnel perform an elaborate peristaltic move- 422 BULLETIN OF MARINE SCIENCE, VOL.
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