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 extraction, 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 progressively 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 derived 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 pressure 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 maneuverable, 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 extensions 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. 49, NO. 1-2, 1991

6 Accelerates to 0.37 5

.•... 0.27 0.16 Rest 0.14 mls Avg. Speed t'Cl Q. 3 0.51 0.22 0.1 0.2 kPa Avg. Pressure •....ll: Q) ;;,•.. rn rn 2 £

-1 o 20 40 60

Elapsed Time (s) Figure 2. Jet and resting pressures in the post-branchial chamber of the mantle cavity of Nautilus. Pressures monitored through a cannula entering the funnel from a pressure transducer, transmitted from the free-moving animal to a remote hydrophone. 'Ventilation at rest' shows pressures generated by the funnel folds, the higher pressures developed in jetting result from contraction of the head retractors; note that forceful jets are often preceded by negative pressures as the head retractors extend to draw a larger volume into the mantle.

ment, pressing water forward and down through the gills and out through the spout. As the wings squeeze forward, water is drawn in behind, to be enclosed when the wings re-extend backwards. Contraction of the different parts of the funnel folds is timed so that there is an almost continuous flow of water through the gills and out through the funnel (Wells and Wells, 1985). The resulting flow, without any movement by the head, produces a jet that will drive the animal backwards at a few centimeters per second. The pressures concerned in the two forms of jet production vary from 0.2 to 6.0 kPa, the former typical of normal quiet ventilation, with no visible head movement, the latter associated with vigorous contraction of the head retractors (Fig. 2). The two pressure extremes correspond to speeds of around 0.04 and 0.4 ms-I (O'Dor et a1., 1990). In Nautilus the weight of the head retractors and funnel muscles is about equal, at 4.5% of the total (shell plus flesh) weight (Chamberlain, 1987). The muscle power potentially available from the two sources could in principle be about the same. While it is evident that the funnel musculature can operate alone, it is unlikely that the head retractors ever do so. The funnel must tense to concentrate and direct the jet stream when the head retractors contract. It seems unlikely that the thin backwardly extending wings contribute to the jet thrust in rapid movements. In extreme cases, head retraction actually expels water from around the WELLS AND O'DOR: EVOLUTION OF JET PROPULSION 423

22 I 20 I I 18 : - 16 ~ 14 h, :3"" 12 I- ..... 0 10 I ", 0 I \ Squid 8 \ ...... 6

4 Salmon 2 ------0 a 0.2 0.4 0.6 0.8 1.2

Speed (ms-1) Figure 3. Cost of transport and jet propulsion, Nautilus and a squid, Illex, compared with salmon, Onchorhynchus. Speed for speed the squid is almost 5 x as expensive as the fish; because the ejectable mass is limited by the volume of the mantle cavity the squid must accelerate a smaller volume of water to a higher velocity than the fish. Being negatively buoyant it is obliged to swim upwards continuously making low speeds particulary uneconomical, Nautilus scores at very low speeds because it is neutrally buoyant and using the ventilation stream to propel itself (after O'Dor et al., 1990). umbilicus, indicating that, far from helping squeeze the water forward, the rearward extensions of the wings cannot actually contain the pressures generated by the head retractors. Jet Propulsion and Oxygen Extraction. - There is a fundamental incompatibility between efficient oxygen uptake and efficient jet propulsion. The former is best served by a system that passes the minimum volume of water through the gills, extracting the maximum possible proportion ofthe available oxygen in the pro- cess. Efficient jet propulsion depends upon ejecting the largest possible mass at the minimum velocity compatible with generating the required thrust (Thrust ex: mv; Energy ex: mv2). Nautilus can extract around 20% of the available oxygen from the ventilation stream at rest, using the wings of the funnel to propel the flow. During active propulsion, using the head retractors, this falls to 5% or less (Wells and Wells, 1985). Under hypoxic conditions, the resting Nautilus can increase extraction consid- erably; removal of up to 50% of the available oxygen has been observed at an ambient oxygen tension of 10 mm Hg. This high level of extraction is, however, associated with a very slow rate of flow and a total oxygen uptake well below that found in an oxygen-rich environment (Wells et al., in press). In exercise the 5% extraction observed provides enough oxygen to fuel jet propulsion at speeds of a few centimeters per second but this rate of extraction cannot, apparently, be maintained as flow rates increase. Above a speed of about 0.16 ms-1 oxygen uptake stops rising; further increases in speed must be fuelled anaerobically (O'Dor et al., 1990). 424 BULLETIN OF MARINE SCIENCE, VOL. 49, NO. 1-2, 1991

5cm

L-.I L--..J 2cm 2cm

Figure 4. Shell shapes ,and body chamber apertures, indicative of ejectable mass, in Nautilus and various ammonites. The genera are, left to right, top row, Oppelia, Amaltheus; bottom row, Macro- cephalites, Eoderoceras, Dactylioceras (the ammonites after Lehmann, 1981).

The Situation in Fossil Forms. - We know little about the soft parts ofthe earliest cephalopods. Fossil shells show no trace of the funnel musculature, and only sometimes, on internal casts, can scars believed to be traces of the head retractors be found (Crick, 1898). The scarcity of such traces is partially explicable when one examines fresh Nautilus shells; the large head retractors do not actually pen- etrate into the shell, but are separated from it by a layer of conchiolin, which peels away, leaving an ill-defined scar. As the animal grows forward the posterior margin becomes obscured. One can guess that extinct forms would have required head retractors irrespective of locomotion, and these would have had to be powerful enough to resist predators trying to pull the creatures out of their shells. The only alternative means of developing a powerful jet would have involved a gross increase in the musculature of the wings. This would not only have been a needless duplication ofpropul.sive musculature already available, but it would have further restricted the ejectabIe mass of fluid in the mantle cavity, a self-defeating exercise. It seems far more probable that the early forms, if they were equipped with funnel wings at all, used these to waft a low pressure ventilation stream over the gills as Nautilus does today. It is possible that the earliest forms did not actively pump water through the mantle cavity, generating a ventilation stream by muscle action. Outside of the cephalopods the usual mechanism of creating a ventilatory current is ciliary. The most compelling reason for supposing that the flow was probably pumped from very early on in the ancestry of cephalopods comes from the structure of the blood system. Nautilus is only remotely related to the coleoids, which appear to have been derived from a rather different group (the orthocerids as opposed to the tarphycerids) of nautilloids (Teichert, 1967). Yet the blood system of Nautilus is laid out on an almost identical plan. There are pumps supplying the gills on the venous side and a massive systemic heart forcing blood down the same trio (cephalic, abdominal and gonadial) of arteries. The implication is that the outline pattern of the blood system was already established in the early ellesmerocerids, with a powerful heart driving blood rapidly through the systemic circulation and accessory pulsatile organs driving blood rapidly through the gills. When one re- WELLS AND O'DOR: EVOLUTION OF JET PROPULSION 425 members that the oxygen content of much of the sea in late Cambrian times was probably less than 30% of that found in the oceans today (Cloud, 1983; Holland, 1984), the existence of a well-developed circulatory system implies a correspond- ingly rapid flow of water across the gills that could not have been supplied by ciliary action alone.

Some Consequences. - The combination of jet propulsion and neutral buoyancy is likely to have been an important factor contributing to the outstanding success of the early cephalopods. Combined with beaks and tentacles, it made them very dangerous predators indeed. And no doubt 0.3 ms-I was a spectacular speed in the early Palaeozoic. Well before the end of that period, with the appearance of a range offish having an inherently more efficient means of rapid swimming (Fig. 3) it was too slow. There was not a lot that any ectocochleate could do about it. The cost of developing the necessary thrust for jet propulsion rises as the square of the jet velocity ( E

a b c

e tr..•...... ,:.:.:::.:.~,::.".. J? d •

f 9

Figure 5. Centers of buoyancy and mass, and consequent likely postures ofectocochleates. The extent of the body chamber is shown stippled in each case. a) Nautilus, b) Dactylioceras, c) Normanites, d) Caloceras, e) Promicroceras, f) Crioceras, g) Ludwigia and h) Sigaloceras (after Trueman, 1941).

speeds of 0.5 ms-1 and, again by analogy with Nautilus. they would have had to achieve that on oxygen debt. A higher level of sustainable activity would have required drastic modifications to the gills and their supporting structures. In Nautilus, the gills are bracketed out from the rear wall of the mantle cavity. They divide the mantle into three cavities, two lateral and a common post-branchial space (Fig. I). In quiet ventilation the gills fill the space between the laterals and the central ventral cavity, so that all of the water pumped by the wings of the funnel passes through them. As jetting becomes more vigorous, oxygen extraction falls, probably because the gills are swept out of the way by the sudden ejection oflarge volumes of water from the lateral chambers (Wells and Wells, 1985). If one supposes that all ectocochleates were built on the same pattern as Nautilus (as argued here; but see "other possibilities" below), the problem posed by a need for an increased oxygen uptake in exercise could not have been solved by increasing the gill area; a larger or more complex gill would have been pushed aside even more rapidly. In coleoids the gills are suspended along their length by a membrane from the wall of the mantle cavity (Fig. 6). This is possible because the water is sucked in at the front and down through the gills by expansion of the mantle wall. A continuous flow is maintained because the expansion of the pre- and post-branchial chambers is slightly out of phase (Fig. 7; Wells and Wells, 1982, 1991). Could the gills of ectocochleate cephalopods have been suspended across the jet stream so as to maintain oxygen uptake during rapid locomotion? The answer, in principle, is "yes." The flow could be drawn in and down through the gills when the head was extended prior to the contraction producing jet thrust. But WELLS AND O'DOR: EVOLUTION OF JET PROPULSION 427

Efferent branchial Afferent branchial

Head Funnel retractor etractor Funnel Suspensory retractor membrane Afferent branchial Efferent branchial Wing of funnel

Figure 6. Gill suspension in a) Octopus, b) Sepia and c) Nautilus. In the coleoids the gill is suspended along its length by a membrane attached to the side or roof of the mantle cavity. In Nautilus there is no such support (a and b after Wells, 1988). only then. There would be no question of a continuous through flow; for that two expandable cavities are required. The head would have to rock back and forth at about the level of the eyes. That would reduce the ejectable mass and is, besides, structurally implausible; what would provide the fulcrum? The combination of penalties, intermittent flow and reduction of jet mass make it rather unlikely that any such system would have been advantageous. It should be noted that both the Nautilus and the coleoid circulatory systems assume more or less continuous flow through the gills. The heartbeat frequency of Nautilus is slower, that of the coleoids faster than the ventilation frequency. For effective oxygen uptake in a pulsed stream they should be synchronous (Wells and Wells, 1982; Wells, 1990). The general conclusion from all these consid- erations is that active ectocochleate cephalopods were all likely to have had mantle cavities, ventilation and jet propulsion systems approximating to the pattern found in Nautilus. The very long body chamber found in some forms would have been filled with guts or gonads but not with propulsive musculature. Other Possibilities. -It is, of course, possible that some ectocochleates were con- structed very differently from Nautilus or the internally-shelled coleoids. Crick (1898) pointed out that internal casts from a wide range of ammonites include crescent-shaped ridges that could indicate the anterior margins of head retractor muscles. Reconstructions like that shown in Figure 8c are based on this evidence and would imply a totally different means of propelling the ventilation/jet stream. Indeed, it is difficult to see how such a stream could have been produced at all, other than by ciliary action, which would imply a slow-moving way of life incompatible with the shell-shape evidence which imples that streamlining and ornamentation were important (Chamberlain, 1976; Chamberlain and Wester- 428 BULLETIN OF MARINE SCIENCE, VOL. 49, NO. 1-2, 1991

Ca) Lateral prebranchial 0.:[ space c..'"

Postbranchial ~ O'T ~I space Cl

/~ ~ Postbranchlal Cbl Lateral prebranchial space 0'1 c..'" Funnel ~OJ

Dorsal

(e) Dorsal mantle space 0] ;\]\),J\ as ~Q. Funnel OJ

L--.....J 1s

Cd)

5s Prebranchial Postbranchial Prebranchial

Figure 7. Ventilation pressure cycles in Octopus and Sepia. Inserts show the position of cannulae in experiments a), b) and c). In Sepia a single pressure transducer was used in a continuous run, with recording switched by tap from a pre- to a post-branchial cannula. a), b), c), from Wells and Smith, 1985; d) from Wells and Wells, 1991. mann, 1976). The evidence for muscle attachments is regarded as equivocal, at least by some authors. Lehmann (1981) has pointed out that the 'flank indenta- tions' on the sides of the living chamber may be retractor muscle scars, a siting that would imply arrangements not only compatible with Nautilus-like layout of the mantle, but also with fossil evidence indicating the extent of the water-filled part of the mantle cavity (Fig. 8a and b). One should note, in passing, that ectocochleate cephalopods have varied so greatly in the past that any generality made about their life-style is unlikely to apply to all. It seems profoundly unlikely that some of the heteromorph ammonites ever indulged in active jet propulsion. If, as Kulicki (1979) and Ward (1987) have suggested, the light shells, siphuncular position and the foliate septa of ammonites allowed more rapid changes in buoyancy than is found in Nautilus, some ofthese animals may have made diurnal vertical migrations without active swimming. Some apparently lack jaws and could have been filter feeders, using expanded gills, or conceivably have fed like Argonauta (despite its popular name, the "Paper Nautilus," no relation of Nautilus and never an ectocochleate; it is an octopod), extending a web on the outside of the shell, to be swept by grasping arms at any chance contact (Fig. 9). When morphologies become as bizarre as those of some of the more extreme heteromorphs, almost anything is possible. WELLS AND O'DOR: EVOLUTION OF JET PROPULSION 429

a b c Ventral unpaired muscle Siphuncle

Mantle cavity

Retractor muscle

'---' 2mm L.j.

Figure 8. Fossil evidence of the body chamber contents of a) Arnioceras and b) Hildoceras. Oe. = Oesophagus. U.j and L.j. = upper and lower beaks. R = Radula. c) is a reconstruction of the layout of the head retractors and gills of a typical ammonite based on apparent muscle scars (see text). a) and b) after Lehmann (1981), c) after Mutvei and Reyment (1973).

A Change of Mechanism. -A large ejectable mass is the key to rapid economical jet propulsion. While the volume of the mantle was restricted by the shell there was no way of significantly improving performance. By the middle of the Pa- laeozoic, harried, we assume, by the rapid evolution of more agile fish (Packard, 1972) several lineages of uncoiled cephalopods were progressively reducing that part of the shell restricting the volume of the mantle (Teichert, 1967). That modification must have required simultaneous progressive development of the musculature and the connective tissue lattice in the mantle, initially to prevent it bulging outwards when the head was drawn down in jetting, but soon to take on a more positive role, contracting to force the water out through the funnel. Eventually this totally replaced the shell retractors as the power source for jet propulsion. The subsequent history of cephalopods jet propulsion has been a matter of a progressive increase in the volume of the mantle and of the mass of the mantle musculature (Wells, 1990). Efficient jet propulsion, as already pointed out, is incompatible with efficient oxygen uptake. The former requires a large mass throughput, the latter is best served by a mechanism that passes a minimum of water through gills that extract a high proportion of the available oxygen. Nautilus has separate mechanisms for the two functions. In coleoids the wings of the funnel no longer stroke the water down through the gills; they function only as flap-valves, channelling the jet stream into the spout of the funnel. The mantle musculature has to serve two functions. There are several consequences. One is a division of the coleoids into those that are specialized for efficient jet propulsion (broadly, the squids) and those that have become specialized for efficient oxygen uptake (octopuses, and, to judge from Sepia, the Sepioidea). The former have large volume mantles, typically elongated because these are streamlined forms, the latter have small rounded bodies min- imizing the length of the flow path and therefore the acceleration that must be given to the ventilatory stream (Wells, 1990; Wells and Wells, 1991). A further development is the division of the mantle musculature into aerobic (high capillary and mitochondrial densities) and anaerobic (low densities) regions, the former in continuous use for ventilation and gentle cruising, the latter to provide maximum burst power for swift attacks and escapes (Bone et aI., 1981). The shell is preserved in the sepioids and gives partial or total neutral buoyancy. In squids and octopuses, neutral buoyancy has been abandoned altogether, in the former in pursuit of streamlining, in the latter, presumably because it is no longer useful, indeed perhaps even disadvantageous to an animal that needs to retain a 430 BULLETIN OF MARINE SCIENCE, VOL. 49, NO. 1-2, 1991

Figure 9. Argonauta, an octopod. The 'shell' is secreted by the first pair of arms, which spread out to cover it with a web. When the web is touched, the fourth arm on the side touched sweeps upwards to grasp potential food (after Young, 1971). grip on the substrate. Where coleoids have, for one reason or another, returned to life-stylesthat would benefit from neutral buoyancy, they have generallyachieved this by replacing sodium with ammonium chloride, a mechanism that leads to rather flabby animals but which, unlike the gas-filled shell, is not limited by an implosion depth (Clarke et aI., 1979). Fish-like Locomotion. -Jet propulsion can produce high acceleration, speed and maneuverability, but the mantle driven jet remains inescapably uneconomical because the volume of water used for reaction mass is limited. Some octopods have evolved a large mass, low velocity system based on arm movements and an umbrella-like web which produces economical locomotion similar to cnidarian medusae (Baldwin and England, 1980; Vecchione, 1990), but they are clearly less well controlled than fish using undulations to sweep a large area with a flat body or tail. Undulatory fish have a distinct economic advantage, although those that swim best forwards typically cannot accelerate well or swim backwards. Many WELLS AND O'DOR: EVOLUTION OF JET PROPULSION 431 coleoids, both among the Sepioidea and the Teuthoidea, have added undulatory fins to their repertoire. A lateral fin can push a large mass of water at low velocity and is even reversible. However, such fins also seem to be a compromise. Small-finned squids like Loligo opalescens use their fins primarily at low speeds and for maneuvering (O'Dor, 1988); their heavy dependence on the jet gives them a cost of transport 4-5 times that ofa comparably sized fish (Fig. 3). Recent studies of Loligoforbesi, with twice the fin area of opalescens, indicate a minimum cost of transport half that of small-finned forms, but both the optimum and maximum speeds are also halved (O'Dor et aI., in press). Rates of undulation in muscular-hydrostat systems (Kier, 1989) appear to be limited so that fins are often rolled-up to reduce drag at maximum speeds (O'Dor, 1988). A unique feature of the jet/fin combination, used effectively to attack undulatory fish which can only make maximum accelerations from a standing start, is the ability to give a jet boost to an already moving platform (Foyle and O'Dor, 1988). Although the greatest asset of the inefficient jet may have been in forcing coleoids to develop and use their brains to control and integrate auxiliary systems, none has so far abandoned the jet completely.

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DATEACCEPTED: November I, 1990.

ADDRESSES:(M.J.W.) Department of Zoology, University of Cambridge, Downing Street, Cambridge. u.K.; (R.K.O.) Department of Biology, Dalhousie University, Halifax. Nova Scotia, Canada.