THE LARGE animals in the sea are almost all vertebrates: fish, turtles and whales. Only one group of invertebrates has produced creatures of comparable size and activity. These are the molluscs, on the face of it an unlikely group to have given rise to some of the ocean’s most outstanding athletes. Yet it did. The cephalopods, a class of animals that includes the squids, cuttlefish and octopuses, are indisputably molluscs. They share a common body plan with clams and snails, but are greatly modified to allow them lifestyles comparable with those of the vertebrates. Between them, the cephalopod molluscs, the fish and the toothed whales constitute a formidable assemblage of predators, eating each other and anyone else available as a source of protein in the sea.
The molluscs established themselves as predators of the midwater zone before the fish. The cephalopods apparently arose from small limpet-like animals that crawled on the seabed. These primitive forerunners of today’s sophisticated predators disputed possession of the late Cambrian sea floor with a range of other animals, most of them armoured, and many, we may safely assume, predatory. What distinguished the early protocephalopod from the rest of the mob was a capacity to secrete gas into the apex of its shell.
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In view of subsequent events it seems reasonable to assume that the benefit derived from the secretion of gas was a lightening of the shell, so that when the little limpet-like protocephalopod withdrew into its shell to escape from would-be predators, the outgoing squirt of water, displaced from the ‘mantle’ cavity housing the gills, carried the creature off the bottom. A useful trick when everyone else is limited to thrashing and gnashing about on the sea floor.
What no doubt originated as a purely defensive tactic rapidly evolved into an outstandingly successful offensive strategy. If it was possible to escape into the water column from the more threatening of the neighbours, it was also possible to fall from above upon the weaker members of the flatlanders below. The foot, liberated from its crawling role, joined the head in developing a series of grasping tentacles and flaps to direct the jet of water ejected from the mantle when the animal withdrew its head. Equipped in this manner, the straight-chambered nau tiloids rapidly came to dominate the seas, diversifying into forms that ranged from a centimetre or so to several metres long.
They also produced coiled forms, a variant that offered several advantages. A coil is easier to steer going backwards, which is the way to get maximum benefit from the jet. It avoids the need to weight the early chambers as the animal grows in order to remain horizontal – necessary if the animal is to jet from place to place rather than simply dodge up and down in the water column. And a coil economises on shell materials, because each whorl serves as the basis for the next.
Nautilus, a coiled form, is the only living cephalopod with an external shell. Rather surprisingly, Nautilus resembles the earliest rather than the majority of later forms, which were predominantly thin-shelled and often highly ornamented. We do not know for certain whether the soft parts of Nautilus resemble those of its extinct ancestors. But it is a fair bet that they do because the apparently primitive anatomy of Nautilus foreshadows most later developments: the living animal would do very nicely as an ancestor for all other living cephalopods. A study of Nautilus should tell us much about the likely physiology of fossil forms quite apart from explaining some of the peculiarities of the design of other living members of the group.
Nautilus produces a jet in two ways. At rest, the ventilation stream, which drives water through the gills and supplies them with oxygen, is produced by the wings of the funnel that directs the jet. The wings extend backwards, almost lining the mantle cavity that houses the gills. To drive the ventilation stream they move in a complex manner, beginning with a wave of contraction that starts close to the umbilicus of the coiled shell, pushing water down through the gills, which divide the mantle cavity into two lateral chambers above and a single chamber below the gills. As the wings squeeze forward pushing water down through the gills, water is also drawn in behind. After completing their forward contraction, the wings ripple backwards along the walls of the mantle and enclose the water that has just been drawn in behind. The forward part of the wings is still expanding while the backward extension is going on, so that an almost continuous stream is maintained across the gills.
This elaborate mechanism functions at very low pressures, the driving force being a pressure in the region of half a centimetre of water. This makes sense. Water is heavy stuff. At best, there is only 1 milligram of oxygen in 100 000 milligrams of water (compared with 1 milligram in 3.5 milligrams of inert gases in air). An ideal ventilatory system moves a minimum of water across the gills, accelerating it as little as possible and extracting the maximum proportion of the available oxygen in the process.
At rest, in well-aerated water, Nautilus can extract about 20 per cent of the available oxygen from the ventilation stream, which is good but by no means exceptional (some fish can extract more than 50 per cent). Where Nautilus scores is in being able to maintain this level of extraction even when the concentrations of oxygen are very low. Indeed, Nautilus becomes more efficient at extracting oxygen as the oxygen content of the water falls. Ventilation slows progressively until in water that is only 5 per cent saturated with oxygen, Nautilus extracts as much as half of the little available. Nautilus can survive and go about its business scavenging food in environments that would be lethal to other cephalopods and most fish.
This is a handy mechanism, but it is hopeless for jet propulsion. What is needed to develop jet thrust is a large ejectable mass and the capacity to accelerate this to a considerable velocity. The pressure that the delicate wings of the funnel can exert is quite inadequate to propel the animal at more than 3 or 4 centimetres per second. To better this, Nautilus reverts to its presumed ancestral escape mechanism, using the retractor muscles anchoring the head and body to the shell to squeeze water out of all parts of the mantle cavity. The retractor (‘shell’) muscles are massive, and can generate pressures in the mantle cavity two orders of magnitude greater than is possible using the wings of the funnel. The result is a tenfold increase in speed.
Thirty centimetres a second was doubtless spectacular early in the Palaeozoic era. It didn’t look so good by the end of the era – by which time fish had made their appearance. Fish had jaws and by the end of the Palaeozoic they had achieved neutral buoyancy by means of a soft, pressurised bladder, a more compact arrangement than an external chambered shell tough enough to resist implosion at depth. And fish had evolved a propulsive system that is inherently sup erior to jet propulsion. The thrust that can be generated by a jet, or by wagging a tail, varies as mass x velocity. But the energy required rises as mV**2. So in energetic terms, it is far cheaper to push back a large mass of fluid at a low velocity than to accelerate a small volume to a high velocity in order to produce the required amount of thrust. The mass that a cephalopod can eject in any one jet cycle is limited by the volume of its mantle cavity. A fish can sweep a large area with its tail, thrusting back at each cycle a volume that can be larger than the volume of the fish itself. At the very least this mechanism is more economical. It probably also gave fish the edge over cephalopods in the matter of speed.
This, then, was the dilemma of the jet set. What had emerged as a winner in the Palaeozoic era turned out to be something of a white elephant in the Mesozoic era. The motor was inherently costly. And it wasn’t fast enough. There was not a lot that the shelled cephalopods could do about it. Nautilus can eject a volume of fluid equal to about 15 per cent of its body weight at each jet cycle. The volume of the mantle cavity is limited by the enclosing shell. The cephalopods could, in principle, achieve minor improvements by streamlining the shell, but a slimmer shell restricts the volume of the mantle cavity, so that any gain achieved by reducing the drag coefficient is offset by a reduction in the ejectable mass.
Under pressure from the fish, the shelled cephalopods did indeed experiment with streamlining the shell. They also made it lighter. In Nautilus, some 90 per cent of the animal’s weight in water is due to the shell, so nearly all of the upthrust generated by the buoyancy mechanism is squandered on the mechanism itself. Any reduction in the weight of the shell increases the weight of the body that can be supported. The difficulty then is that the rather fragile shell can no longer resist the pressures of living at great depths. Nautilus can live down to about 800 metres, but below that the shell collapses. Some of the ammonites that evolved from the nautiloids had paper-thin shells. Clever architecture, including some very fancy fan-vaulting, made these shells very strong for their weight, but even so, they were mostly limited to water that was very shallow by the standards of Nautilus.
The basic problem remained; a cephalopod with an external shell could do very little to increase the ejectable mass. Elongation of the mantle cavity – some of the ammonites had body chambers that extended for more than the whole circumference of the shell – was no solution because the only way such an animal could eject the water forcefully would be by pulling in its head like a piston, hardly a credible mechanism for an animal that was to have any control over where it was going. In any case, the centre of gravity of such forms would be close to the centre of buoyancy, so that any considerable thrust would have spun the animal like a Catherine wheel. A long thin mantle cavity would be equally ill-adapted for efficient ventilation. We must conclude that the long thin mantle cavity of many ammonites was filled with guts and gonads rather than water and that such forms would have been weaker swimmers than species with short wide body chambers.
The only possible means of increasing the ejectable mass was to extend the mantle cavity beyond the confines of the shell, either by growing out beyond it or by eliminating the shell along the floor of the mantle cavity. Cephalopods with these sorts of modification begin to crop up in the fossil record during the latter part of the Palaeozoic era. The shell, no longer protective, was at first retained as a buoyancy device and then almost abandoned. Modern squid retain the shell only in the form of a chitinous rod that stiffens the back of the elongated abdomen.
The change involved far more than loss of armour. An entirely new set of muscles became involved in jet propulsion. The wall of the mantle, freed from the enclosing shell, became capable of expansion and contraction, drawing water into the now much enlarged mantle cavity and ejecting it through the funnel. The capacity of the mantle increased from a maximum of around 15 per cent of the body weight (excluding the shell) in Nautilus to 25 per cent in the cuttlefish Sepia, and to almost 60 per cent in active squid such as Loligo. There was a corresponding increase in the volume of the mantle muscles. In Nautilus, the head retractors make up about 9 per cent of the body (flesh) weight. In Sepia, the muscles of the mantle form some 30 per cent of the body weight; and in squid, this increases to about 40 per cent. Deprived of their ancestral function, the head retractors persisted as necessary anchors between the head and the increasingly powerful propulsive mechanism in the abdomen that would otherwise threaten to snap the animals off at the neck at times of maximum acceleration.
Progressive reduction of the shell meant loss of neutral buoyancy. This in turn meant that the gains from an increased mantle capacity tended to be in speed rather than economy. For a squid must swim continuously or it will sink. The neutrally buoyant Nautilus is economical provided that it moves slowly; indeed, at slow speeds it is fully competitive with fish in terms of energy expenditure. Squid are hopelessly inefficient at slow speeds because almost all their effort then goes into keeping the animals up rather than moving forward. But even at its ‘best’ speed (50 to 75 centimetres per second for an animal weighing half a kilogram) a squid consumes almost four times as much fuel as a well streamlined, neutrally buoyant fish.
As the remains of the shell were progressively enclosed the new ‘shell-less’ cephalopods slimmed down to finely streamlined, almost fish-like forms. They also developed fins, lateral outgrowths from the sides of the abdomen that not only added control surfaces but also introduced a means of locomotion that freed them from the restraint imposed by jet propulsion. Cephalopods began to swim like fish, undulating the fins to develop thrust far more economically than by jet. Routine locomotion by many cephalopods – squid, cuttlefish and octopuses – now depends as much on fins, or crawling with the arms, as it does on jet propulsion.
Other cephalopods, and in particular those living in the open oceans and deep water where food is comparatively scarce, redeveloped neutral buoyancy. Having burned their boats in the matter of the shell, the oceanic squid exploited a mechanism that is widespread in planktonic animals. They altered the ionic content of their tissues, notably by hanging onto ammonia, which they produced as the end product of protein metabolism, and using this to displace sodium ions. Ammonium chloride is lighter than sodium chloride, and seawater is a solution mostly of sodium chloride. The advantage of such a mechanism is that it is pressure-proof, so that it will work satisfactorily in the deep sea, below the depth to which any shelled form could penetrate. Moreover, none of the buoyancy gained is squandered on supporting the mechanism itself.
The bad news is that ammonium chloride is toxic; so the buoyant solution had to be isolated in regions of specialised cells, forming pockets in the musculature, or retained in enormously enlarged kidneys. A second snag is that the buoyancy gain is minimal; proteinaceous body tissue has a density of around 1.33 grams per cubic centimetre, compared with oceanic sea water at around 1.024; the fluid in the ammonia-rich pockets of squid has a density of about 1.010. So squid need an awful lot of it. Carried on to the point where totally neutral buoyancy is achieved, it makes them distinctly flabby. In all this, the cephalopods always retained the jet. Uneconomic it may be, but it gives cephalopods a range of capabilities that fish do not possess. A squid with a jet and a directive funnel is almost as fast forwards as backwards. The unpredictability of the escape route that a cephalopod will take when threatened must be a continual source of frustration to would-be predators. The jet is handy for other purposes too. It can be used to dig holes or to flush out prey, to spread a smokescreen or eject a blob of ‘ink’ as a decoy (a further line of defence that has no parallel in fish), to propel a sudden pounce on prey, or even (in octopuses) to aerate brooded eggs.
Jet propulsion was one of the earliest forms of locomotion. Jellyfish moved in this way, pulsating the bell, before many other sorts of animal were even a gleam in the creator’s eye, and the nautiloids, as we have seen, were the first large midwater predators. But many living cephalopods have abandoned jet propulsion except for emergencies. The jet set, after tinkering with the motor for millions of years now seems to be doing its best to develop less expensive means of getting about. There must be a lesson in this somewhere.
Martin Wells is reader in the department of zoology at the University of Cambridge.