A Broad Brush History of the Cephalopoda

<< Cephalopod Articles | By Dr. Neale Monks author of Ammonites

Cephalopods are one of the few animal groups that are both diverse and ecologically important today and yet have an extensive fossil record going back almost to the very beginnings of complex animal life during the Cambrian period around 550 million years ago. However, understanding the evolution isn't simply a case of using the fossils to build family trees culminating in the living species, because the groups of cephalopods most richly represented in the fossil record are ones with few, if any, living species! When discussing cephalopod evolution it is important to realise that they haven't evolved in a linear way from some primitive nautilus-like creature in the Cambrian through to the modern and undeniably sophisticated squids and octopuses. It is much better to think about the cephalopods as comprising three anatomically and ecologically very different groups—the Nautiloidea, Ammonoidea and Coleoidea—each of which has adapted and evolved independently of the other groups and experienced different degrees of success and failure.

The Nautiloidea

Nautilus © James B. Wood

Nautiluses are the most primitive cephalopod group and all have relatively simple, buoyant chambered shells within which the soft body is protected. The high point of nautilus evolution would appear to be during the Paleozoic from about Ordovician and Silurian periods (about 505 to 408 million years ago). During this time giant straight-shelled nautiluses were the only really large animals able to actively swim above the sea floor, sharks were still quite small animals and bony fish hadn't yet become neutrally buoyant. As such these animals must have been the great white sharks of their day, probably eating anything they could find and overpower, but some may also have eaten the swarms of midwater crustaceans rather like whales taking krill today.

Two genera of nautilus survive to the present day, Nautilus and Allonautilus, but it isn't at all obvious whether these living nautiluses are representative of their extinct kin as well. For a start the living species belong to a single family, the Nautilidae, that doesn't go back any further than the Late Triassic (about 215 million years ago); the greatest variety of nautiluses had already lived and died long before then. Ecologically the living species seem to be quite specialised

Nautilus fossil - Eutrephoceras bouchardianus

Cretaceous nautilus (E. bouchardianus) fossil © NHM

too, at least compared to all other living cephalopods. For example they grow very slowly and reproduce slowly; they are tolerant of low oxygen conditions (something that kills other cephalopods very quickly); and they are opportunistic feeders happily scavenging carrion rather than active predators. On the other hand, the living species of nautilus do have some features typical of the primitive molluscs from which the cephalopods evolved, such as a robust shell and multiple pairs of gills. The coiled shell divided into gas-filled chambers and providing both buoyancy and protection is at least superficially similar to those possessed by another cephalopod group, the Ammonoidea, which will be discussed later on. But it is important to note that coiling evolved independently in the two groups. The first ammonites, like the early nautiluses, had straight shells and in fact it seems most probable that both ammonites and coleoids evolved from the straight-shelled nautiluses.

Even after their heyday in the Paleozoic, nautiluses have remained conspicuous if not actually important components of marine communities. Several new sorts evolved during the Mesozoic and Tertiary periods alongside the various ammonite and coleoid groups. Among these new types was the genus Aturia, comprising nautiluses with complex, highly folded sutures, very robust and conical siphuncles, and laterally compressed shells. These are common in Tertiary rocks as young as those as the Miocene (about 5 million years old) indicating that while the mass extinctions at the end of the Cretaceous were bad news for the

Pin-hole eye of Nautilus © James B. Wood

ammonites, the nautiluses sailed through them seemingly unharmed. Indeed, there is quite a flurry of new nautilus types immediately after the Cretaceous-Tertiary boundary, suggesting that to some degree at least nautiluses were able to take advantage of the niches left empty by the extinction of the ammonites.

Nautiluses are currently confined to the tropical Indo-West Pacific region although the odd specimen can drift much further away (for example, a live specimen has been found on the coast of Japan). They are not particularly diverse at the species level, with about five species divided into two genera, Nautilus and Allonautilus, but individual populations around each group of islands do seem to be quite distinct. It seems probable that the various populations were able to mix more easily in the recent past when sea level was lower than it is now, but in the last hundred thousand years sea level as fluctuated significantly, and right now the populations are more or less completely isolated. In short, the nautiluses are diversifying and evolving into new kinds, like Darwin's famous finches stranded on the various Galapagos Islands.

The Ammonoidea

Ammonites are the best-known cephalopod fossils and for a very long period of time, from the Devonian through to the Cretaceous (408 to 65 million years ago) they were major players in most marine ecosystems. It is tempting to think that they occupied the sorts of niches that fishes do today, but that is probably unwise. To begin with there were plenty of fishes around during this time too, particularly by the Mesozoic when many modern groups of cartilaginous and teleost fishes made their appearance. In addition, the ammonite body plan offers a different set of advantages and disadvantages compared with a bony fish, for example.

Heteromorph ammonite, Hamites maximus. These shells are often helical in the juvenile phase and planar when mature. © Neale Monks

The buoyant shell means that swimming is much easier with little energy needing to be expended to maintain position in the water column against gravity, and a shell with ribs and spines can offer some defense against many predators. But on the other hand a shell is a bulky, awkward structure to carry around ruling out niches were a flexible body or tight maneuvering is needed. Pumping water in and out of a space within a shell, as ammonites and other cephalopods need to do to respire, is fine, but for swimming this sort of "jet propulsion" is

Hamites incurvatus is planar throughout growth. © Neale Monks

far from ideal. While a fish can move more water by having a larger fin with stronger muscles, and therefore swim more powerfully, a cephalopod needs to make its entire body bigger since it needs to increase the volume sucked into its mantle cavity if it is to squeeze out more water and so swim faster and further. With ammonites, not only does the body need to get bigger, but also so would the shell if it is to remain neutrally buoyant, and the bigger the animal the more drag it will experience. Worse still, the coiled shells of ammonites are not only an unstreamlined shape to begin with, but those with ribs and spines for defense would make swimming fast practically impossible.

So whatever ammonites were, for the most part at least they weren't fish analogues. Much more likely is that they occupied a variety of niches comparable to those occupied by modern crustaceans such as crabs and lobsters, and molluscs like the plankton-feeding cranchid squids. There are a few ammonites that might have been active, open water predators, such as Placenticeras, which is quite smooth and streamlined, and does turn up in offshore sediments. But did it cruise the sea in schools like modern mackerel or jacks? Probably not: using its jet propulsion it would have swam backwards, with its head and arms pointing the wrong way to catch prey. Unlike modern squids it lacked fins for forwards swimming, at best it could have maintained its position using its jet, and waited for prey to swim into range of its arms.

Ammonite evolution is a parade of ostentatious success and catastrophic failures. Some groups never really amounted to much, like the Anarcestina, and only lasted a few million years before going extinct. Others were long-lived but conservative groups, such as the Phylloceratina, which lasted from the Triassic through to the end of the Cretaceous (248 to 65 million years ago). Yet others, exemplified by the Ammonitina and the Ancyloceratina, were both long-lived and very diverse. With each mass extinction even, and there have been many, some few ammonites survived and gave rise to a whole new assemblage of forms. They did of course fail to do so after the end Cretaceous extinctions for reasons that remain controversial. There were probably a combination of factors at work including the appearance of different sorts of predators better able to break through ammonite shells, climate and sea-level change, and perhaps a catastrophic collapse in the plankton on which baby ammonites appear to have fed.

Caribbean Reef Squid in Bonaire Marine Park. © James B. Wood

The Coleoidea

The final of the three groups of cephalopods appeared at about the same time as the ammonites and diversified alongside them. It is absolutely crucial to recognise that coleoids didn't replace ammonites or that ammonites in some way out-competed coleoids during the Mesozoic. While the two groups do seem to have some anatomical and perhaps developmental traits in common that set them apart from the nautiluses, in many ways they are very different groups. While ammonites seem all to have relied on their shells for defense was well as buoyancy, coleoids had internal shells useless as a defense. A few coleoid groups have also discarded the shell as a buoyancy aid. While these groups—the squids and the octopuses—happen to be the dominant cephalopods in the modern seas, coleoid evolution didn't lead inexorably towards this state. The belemnites, one of the most successful groups of coleoids, had well developed chambered shells, and were very abundant in the seas of the Jurassic and Cretaceous (213 to 65 million years ago) right alongside the ammonites. In the Tertiary there appeared several different groups of coleoid that each had highly modified but still chambered and buoyant shells. Among these, two groups survive to the present day and both are ecologically important and unquestionably successful: these are the shallow water cuttlefishes, and deep-water spirula.

We noted at the beginning of this essay that the buoyant shell is what allowed cephalopods to become active predators at a time when most other

Cuttlefish, Sepia pharaonis. © James B. Wood

Sepia (cuttlefish) Fossil © NHM

organisms were down on the sea floor. So why did the squids and octopuses lose their buoyant shells? This is an exceedingly tricky question to answer because the animals with uncalcified shells, if they have shells at all, are the animals least likely to leave behind a fossil record. As a result, we know virtually nothing about fossil octopuses. There are only a couple of body specimens known from the Mesozoic, Argonaut-like egg case fossils from the Oligocene, and Octopus-like borings into clam shells from the Miocene. A little more is known about the squids thanks to their slightly more durable shells, claws and statoliths. Another complicating factor is that the majority of squids and octopuses today, and perhaps in the past as well, were offshore and deep-water animals, and fossils from such environments only very rarely end up on land where geologists can find them. Getting live specimens from deep water is difficult—imagine trying to collect fossils from the bottom of the sea!

Octopuses (and their close relatives the vampyromorphs) seem to have lost their shells independently of the shell reduction seen in squids. Vampyromorphs, represented today by Vampyroteuthis, were moderately diverse during the Jurassic and many of the so-

called Jurassic squids are in fact vampyromorphs (such as Belemnoteuthis and Plesioteuthis). The Jurassic vampyromorphs had shells with chambers that presumably offered neutral buoyancy, but later species this function was lost and the shell became uncalcified. Octopuses diverged from the vampyromorphs during the Late Jurassic (about 140 million years ago) as far as we can tell—but the fossil record is too patchy to make this estimate anything more than provisional. In some ways octopuses can be thought of as vampyromorphs that have lost their shells more or less completely. Comparisons of the mitochondrial DNA of various types of living cephalopod also seems to support a closer relationship between the octopuses and vampyromorphs that either has with the squids, spirulas or cuttlefishes. Of the two octopods groups—the Cirrata and the Incirrata—it isn't at all obvious which gave rise to which, and why the octopuses lost their shells so completely is obscure.

The squids have shells that no longer provide buoyancy but unlike the situation with octopuses, the squids have retained their shell for other purposes. Most crucially the shell provides rigidity to the body and support for the musculature, essential functions in these powerful, fast moving animals. Confusion exists over whether or not the two groups of squids, the Oegopsida and the Myopsida, are more closely related to one another than either are to the cuttlefishes or spirulas. The

morphological evidence is equivocal on this, but the molecular data appears to support a close relationship between the myopsids and oegopsids. This would imply that the ancestors of all modern squids had some sort of chambered, calcified shell probably most similar in form to that of the modern spirula except straight rather than coiled.

But why are octopus and especially squid shells unchambered when neutral buoyancy would be useful to active, midwater animals? There are three obvious possibilities. The first is that the early squids and octopuses inhabited deep water where maintaining a gas-filled shell is difficult: the gases needed to fill the chamber won't diffuse out of the blood fast enough, and water pressure tends to crush any gas-filled shell anyway. Nautilus can't survive at depths in excess of 500 m (it implodes), and the spirula is found at depths of 800 to 1000 m. Many squids and octopuses inhabit far deeper waters than this, and if this was the habitat they evolved in, then perhaps there was no way the shell could be kept. Interestingly, many deep-water fishes have no swim bladder, probably for the same reasons. Another possibility is that they passed through a bottom-dwelling stage in their evolution. Many modern octopuses are active burrowers and perhaps a shell is redundant, or even a handicap, to an animal that inhabits burrows and caves. Also, being crawlers rather than swimmers, a buoyant shell was probably unnecessary, in the same way that benthic fish like gobies and flounders have reduced swim bladders. Finally, it may be that squids and octopuses lost their buoyant shells in response to predation pressure from echolocating predators like dolphins. A hollow shell will return a very obvious echo, making the bearers of such shells easy targets. The extra costs involved in having to swim without the benefit of neutral buoyancy may be offset by the improved survivability against these sorts of predators. It is certainly noticeable that until the Miocene when echolocating cetaceans diversified, there were many more kinds of cephalopod with chambered shells than there are today.

Conclusion

Cephalopod evolution is not a linear progression from nautilus to spirula to cuttlefish and to squid as it is often portrayed in textbooks. The three main groups have all been successful and diverse but in obviously different ways, and with only a few nautiluses and no ammonites living today it is impossible to make ecological comparisons between them with any degree of certainty.

A crucial question that needs to be answered is did the squids and octopuses evolved in deep water and expanded into shallow water later on? This could explain why they have unchambered shells, and might also explain why they survived the Cretaceous-Tertiary mass extinctions when so many shallow water groups (including the ammonites) succumbed. In a deep-water refuge they could have been protected from extreme changes in temperature or pH, and perhaps able to use food sources less sensitive to collapses in phytoplankton or zooplankton populations. A deep-water stage in their evolution raises an interesting contradiction though: the complex eyes and visual modes of communication employed by squids and octopuses aren't typical of deep-water invertebrates or even fish, which tend to emphasis the senses of touch and olfaction instead.

If they did evolve in deep water, then what was the cause of their expansion into shallow water habitats? Squids and octopuses are often talked about as "invertebrate fish" but if this were true, then surely the bony fishes would have already occupied the niches the squids and octopuses might occupy? That the squids and octopuses are in shallow waters would seem to imply that there isn't that much overlap between them and the fishes, however attractive such an idea might be. So what is it that squids and octopuses had going for them that allowed them to carve out entirely new ways of making a living in coastal waters and the upper levels of the open sea? Their extraordinary physiology, combining rapid growth and large size with plastic behaviour and a sophisticated sensory system, must be significant, but how?

Cephalopods may have a good fossil record, and may be among the most studied invertebrates for a variety of reasons from fisheries management through to neurophysiology, but in many ways they remain a complete enigma. Just how does evolution turn a floating slug into a racing snail? And why?

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