I’ve never seen a living argonaut. Few people have. In a rare sighting in October 2012, fishermen accidentally caught a female argonaut while hunting for squid a few miles off the coast of Los Angeles. They brought the strange creature back to shore and gave it to a local aquarium. It was unusual for this tropical species to show up in temperate Californian waters. Staff at the Cabrillo Marine Aquarium assumed that she had been carried on a current sweeping up from the south and carefully placed her in a warm-water tank. For some time, the exhausted animal lay helplessly at the bottom and the aquarium keepers feared the worst. Then one of them thought to give her a helping hand towards the water surface. After that, the argonaut perked up, and started swimming around her captive home; she eventually began to eat, grabbing morsels of fish and shrimp offered to her.
A video posted online shows the captive Californian argonaut. Hovering in the water, her shell is iridescent with a bronzy-silver gleam and for the first few seconds it’s difficult to make out the animal inside. Then all of a sudden she pops out, revealing herself to be a delicate, shiny little octopus. She pulls out her eight arms, grabs hold of her shell and deftly spins it round before climbing back inside.
Argonauts are the only octopuses that live inside a shell. All the other members of the order Octopoda, around 300 in total, have embraced a soft, naked life. Now and then you might spot a common octopus peeping out from inside an empty clam shell. A video clip went viral a few years ago of an octopus in Indonesia picking up half a coconut shell and strutting off across the seabed, using its arms as legs. When it comes to full-time shell-living, though, it’s just the four members of the genus Argonauta: the Greater, Rough-keeled, Brown and Tuberculated Argonauts. They all look quite alike, with pale and thin shells, covered in ridges and rows of nodules. Depending on the species, their shells can be between five and thirty centimetres (two and twelve inches) across, while the animals inside are considerably smaller. Throughout their lives they cruise the upper highways of tropical and subtropical seas, way above the heads of their octopoid relatives, which mostly live close to the seabed, lolloping and swimming along but rarely venturing too far up into open water.
After a week of life in captivity at the Cabrillo aquarium, the argonaut gave everyone a big surprise. She was joined in her tank by thousands of tiny argonauts. It turns out she had been carrying fertilised eggs, and now they were starting to hatch.
It was all hands on deck as helpers were drafted in to count the new arrivals. Clerical staff were brought out from behind their desks, and visiting schoolkids were given a taste of scientific research. Over a course of a few days, the argonaut released a total of 22,272 minute hatchlings, each one only a millimetre across. Other videos, this time shot down a microscope, show some of the new argonauts. The twitching oval blobs are mostly transparent, with two big, dark eyes and a covering of spots that expand and contract; one minute they are patterned like a giraffe, the next they are peppered with tiny black dots. The flickering colours are made by chromatophores, cells embedded in the mantle that are filled with pigment granules and are concealed or revealed by minute muscles relaxing or contracting. The infant argonaut grapples with zooplankton and uses its little arms to shovel them into its mouth; it’s the first time such a tiny argonaut has been caught on camera tucking into its food.
Sadly, though, the Californian argonaut and her plentiful offspring didn’t survive more than a few weeks in captivity. The aquarium keepers couldn’t easily have returned her to the sea because the warm water current that delivered her to California had stopped and they were a long way from her normal tropical habitat. At around the same time, empty argonaut shells were found washed up on nearby beaches, suggesting there had been some sort of mass stranding. Even if the captive argonaut had been left at sea she might not have survived. At least this nomad had helped researchers gain new insights into these most enigmatic creatures.
People have known about and puzzled over argonauts for millennia. Two questions have confounded many great minds: what purpose does the argonaut’s shell serve, and where do their shells come from?
The name ‘argonaut’ stems from Greek mythology, and the band of heroes – the original Argonauts – who sailed on the ship Argo with Jason in search of the Golden Fleece. It was the Greek philosopher Aristotle who first wrote about their molluscan counterparts. He suggested they use their shells as boats to float on the surface of the sea, with their arms as oars to row themselves along, or two arms flattened and hoisted up as sails. The story was passed on and retold for centuries by naturalists, and writers who professed to have seen this strange scene for themselves. The sailing octopuses appear in Jules Verne’s 1870 novel Twenty Thousand Leagues Under the Sea. While held captive aboard Captain Nemo’s submarine, the Nautilus, marine biologist Professor Aronnax ponders the peculiar sight of hundreds of argonauts sailing across the waves, all holding their arms in the air like flapping ears.
An alternative common name for argonauts is the paper nautilus, because their light, papery shells look a little like those of the chambered nautilus. As this name suggests, nautiluses have shells that are divided into chambers (argonaut shells, by contrast, have no inner chambers). As they grow, expanding their shells from the open end, nautiluses inch their body forwards, and periodically seal a chamber off behind them. A tube running between the chambers, called the siphuncle, then empties liquid from the new chamber by osmosis, and gases diffuse in. Nautiluses can adjust the fluid levels inside their shells, like a submarine’s ballast tanks, controlling their buoyancy and reducing the energy demands of active swimming. Like other cephalopods, nautiluses swim by jet propulsion in a two-stroke system: water is sucked inside the shell, then squeezed out through a funnel. Shifting the position of the funnel controls their direction to some extent; nautiluses swim hesitantly forwards but can scoot away backwards at much greater speed. When they feel threatened, they can withdraw inside their shells, and shut the opening with a leathery trapdoor called a hood.
On the inside nautilus shells are lined with mother-of-pearl, giving them their other common name, the pearly nautilus. On the outside, they’re decorated with ginger tiger stripes across the top, with some that fade to white underneath, as if on being dipped in the sea their markings had started washing off. There are four recognised species in the Nautilus genus, including the Belly-button Nautilus and the White-patch Nautilus. Two other species were shuffled across into a new genus, Allonautilus, because when living specimens finally showed up a few years ago they were thought to be rather too different from the rest. All of them have around 90 slim tentacles – the most of any living cephalopod – making them look like they’re eating a mouthful of spaghetti. They occupy tracts of deep, tropical waters, in the Indian and Pacific Oceans, and are rarely seen alive. When they die their empty shells bob to the surface and can drift to distant shores.
Empty shells were all people knew of nautiluses for a long time. Collectors adored their shininess and elegant whorls, and naturalists were desperate to get their hands on a complete specimen, soft parts and all. Paper nautilus shells, on the other hand, did occasionally show up with something living inside them, but this didn’t stop naturalists arguing over the identity of these little creatures.
On an ill-fated 1816 expedition to find the source of the River Congo, British naturalist John Cranch was fishing for specimens from the Gulf of Guinea off West Africa when he found several argonaut shells, complete with living occupants. They survived on board in a bucket of seawater for several days while Cranch observed them. He saw they could come all the way out of their shells, if they wanted to, and otherwise looked and behaved like octopuses: they had suckers that stuck to the side of the bucket, they swam around using a jet of water and their skin changed colour.
All of this was later reported by William Leach, curator of zoology at the British Museum, because Cranch himself died of fever, along with most of the crew, and never made it back from Africa. In honour of his lost friend, Leach named the argonaut species Ocythoe cranchi, but this was applied only to the soft animals, not the shells they were found in. Many eminent naturalists believed the octopuses didn’t belong with the shell but had killed and devoured the original occupant before seizing their vessel and sailing off. In their minds the octopuses were nothing but parasites.
Carl Linnaeus had named the shells Argonauta argo back in 1758, in the tenth edition of his book Systema Naturae, and in 1814 Constantine Samuel Rafinesque assigned the name Ocythoe antiquorum to the allegedly parasitic animals that were often found inside. John Cranch’s was a new species of parasitic octopus.
For a long time, a living specimen of the shell-making argonaut itself remained unknown. Presumably they were lurking down in the depths somewhere; perhaps they were some other kind of nautilus. The fact that none had been found wasn’t seen as a major problem, though; after all, chambered nautiluses were very rarely seen alive, but their empty shells were fairly common.
In 1828, English naturalist William Broderip reported in the Zoological Journal that a French collector in Marseille claimed to have found a real argonaut, not a hitch-hiking Ocythoe octopus. I can sense Broderip’s eyebrows twitching as he wrote this, and he stayed on the fence, pointing out that much remained to be known before coming down firmly on either side. But he still took a punt that in the long run the octopuses would probably be revealed as pirates, and not the industrious shipwrights of what he called ‘fairy boats’.
The idea of octopuses sailing around in stolen shells may sound like a fanciful Just So Story, but there are some even stranger ideas floating around that have made scientists stop and think. Rather than snatching shells from living species, maybe argonauts hijacked them from far more ancient creatures?
The small collection of living nautilus species is all that remains of an immense cephalopod dynasty. In modern seas, the most common cephalopods are the ones with no external shells, the octopuses, squid and cuttlefish. But in times gone by it was the shelled cephalopods that reigned supreme. Masses of animals that looked a lot like nautiluses romped through the oceans for hundreds of millions of years. Within that group, the most abundant and diverse of them all were the ammonites, and there were some that looked so eerily similar to argonauts, you might be persuaded they were cast from the same mould. By the late nineteenth century, a distinctly offbeat idea had come to light. What if naked octopuses originally borrowed or stole shells from ammonites? Did argonauts learn how to make shells by copying their ancient relatives?
This theory was first proposed in 1888 by German geologist Gustav Steinmann; it was revisited in 1923 by Swiss palaeontologist Adolf Naef, then again in the 1990s by Zeev Lewy from the Geological Society of Israel. They all imagined the ancestors of modern argonauts to have started out hiding inside empty ammonite shells. Then the argonauts somehow evolved the ability to fix up their borrowed shells, to mend holes and cracks. As the argonauts got better and better at repairing shells they eventually no longer needed a template at all, and could merrily continue shell-making without having to find an ammonite shell first.
Lewy went a step further, proposing that argonauts were in fact scavengers of recently dead ammonites, which he rather charmingly referred to as ‘post-necrotic floaters’. In other words the ammonite shell, complete with dead animal inside, floated to the sea surface and drifted around for a while. Lewy suggested that naked argonaut ancestors laid their eggs inside these post-necrotic floaters, leaving the new hatchlings to slowly eat their dead hosts and ultimately occupy the vacated shell.
To find out if there is any truth in these ideas and see if there is a link between argonauts and ammonites, we should jump back in time half a billion years to see where this all began. Down at the base of the cephalopod evolutionary tree sits a little creature that lived towards the end of the Cambrian. It was about the size of a pinky toe and wore a slender and slightly bent shell like a wizard’s hat. Charles Doolittle Walcott, of Burgess Shale fame, was the first to describe fossils of these animals (though they were from later deposits), and he named them Plectronoceras.
Plectronoceras is the oldest undisputed cephalopod (strange creatures called Nectocaris from the Burgess Shale itself could be cephalopods, although not everyone agrees on that). Their shells were divided into chambers, like nautiluses, and they may have spent much of their lives skipping across the seabed or wafting through shallow seas as part of the plankton. Following on from these modest drifters there were far more impressive, not to mention scarier, cephalopods to come.
Starting around 485 million years ago, the Ordovician was the next major stage in Earth’s history. The planet was a strange place compared to the way things are now. Temperatures were much higher, as were carbon dioxide levels, and most of the landmasses were clumped together into a massive super-continent, Gondwana, but nothing much lived there. Life was still largely confined to the oceans, where there was a mixture of living things that we could recognise today, plus a range of other, bizarre creatures.
Trilobites scuttled across the seabed; bivalves and brachiopods stayed put as they sifted the water for food; gastropods ambled past fronds of red and green seaweeds and colonies of coral. Above the seabed, early chordates called conodonts wriggled their eel-like bodies and gnawed at their food with the sharpest teeth that ever evolved; floating through the water were colonial creatures called graptolites that looked like delicate, saw-toothed tuning forks. For all of these creatures, one of the most dangerous things they were likely to encounter in Ordovician seas was an enormous shelled cephalopod.
The unassuming Cambrian cephalopod lineage went on to flourish in the Ordovician. They evolved into masses of new groups; some were tightly coiled, others had shells as straight as pencils. Incomplete remains have been found of gigantic straight shells from a creature named Cameroceras. Estimates of their full size range up to an astonishing 10 metres (more than 30 feet), as long as a double-decker London bus. These were formidable beasts, like a primeval apparition of a Colossal Squid, the main difference being that these ancient creatures lived inside the longest seashells ever to exist.
It’s generally thought that Cameroceras may have spent a good deal of time resting close to the seabed, pulling itself along with a cluster of arms and scooping prey into its mouth. Other straight-shelled cephalopods would have hung in the water with their heads down, grabbing prey from the bottom. Some evolved counterweights at the ends of their long shells and swam horizontally. Like giant spears, they could have shot through the oceans in pursuit of prey. Whichever way you look at it, the Ordovician saw the rise of the cephalopods.
Towards the end of this period, the super-continent Gondwana drifted towards the South Pole, giant ice sheets spread across the land and Earth fell into a very deep ice age. Sea levels dropped, and continental shelves were drained of their shallow seas, depriving much marine life of its habitat and triggering a mass extinction. Over half of all marine invertebrates were wiped out, but cephalopods were among the survivors.
For tens of millions of years, cephalopods waxed and waned many times. Throughout the Silurian and into the Devonian periods, they went through repeated pulses of decline but always picked themselves up and carried on, recovering their abundance and diversity. It was in the early part of the Devonian, around 400 million years ago, that a series of important new branches sprouted in the cephalopod evolutionary tree. There were the Nautilida or nautilids that led on to the modern nautiluses. The coleoids showed up too, which eventually gave rise to the living octopuses, cuttlefish and squid. The third major lineage of cephalopods to emerge in the Devonian went on to produce some of the most supreme sea creatures of all time: the ammonites.
Chronoscopes and thunderstones
If you fancy getting your hands on your very own ancient, extinct creature I’d recommend looking for an ammonite. Fossil ammonites are hugely abundant and widespread, not to mention very lovely objects. I have several ammonites that were found and given to me by Kate, my geologist sister, who knows only too well my soft spot for interesting things from the sea. My favourite in this little collection is an intricate, tightly coiled shell covered in delicate ridges, and just the right size to cover up with my thumb. It got trapped in a layer of black silty mud that eventually turned to mudstone and became part of the crumbly cliffs of Kimmeridge Bay on England’s south coast. This animal swam through the seas 150 million years ago and now sits on my desk, where from time to time it helps to straighten out my sense of perspective on the world, and of time passing.
Because they’re so common and easy to find, fossil ammonites have been wending their way into human lives for thousands of years, sometimes without people even realising. Walk through the Grand Arcade shopping centre in my home town of Cambridge, England and look down, and you’ll spot ancient spirals in the polished limestone tiles beneath your feet. Long before anyone knew their true origins, and way before they began appearing in shop floors, people across the globe found these strange coiling stones and wondered what they were.
In Europe, fossil ammonites were often called snakestones, with accompanying legends to explain how they were made. Often it was a story about a saint, who went around turning real snakes into stone then hurling them off cliffs. Snakestones were widely believed to cure snakebites and all sorts of other conditions, from human impotence to cramp in cows.
Ancient Romans believed they would see into the future if they slept with a golden ammonite under their pillow. The Blackfoot people of North America thought ammonites looked like sleeping bison and called them buffalo stones; finding one before a journey was a good omen. Black ammonites from the Gandaki River in the Himalayas are called shaligrams. They are worshipped in monasteries and temples as manifestations of the Hindu god Vishnu, and people on their deathbeds drink water steeped in these sacred stones to free them of their sins.
Similar beliefs surround belemnites. These extinct relatives of the ammonites were coleoids, along with octopuses and squid, and while they were quite squiddy in their external appearance they had an internal, bullet-shaped shell. Fossil belemnite shells, known as thunderstones, were thought to be created when thunderbolts struck the ground, and they too were used as a cure for snakebites, as well as protecting a house from getting hit by lightning when they were placed on a windowsill. In Swedish folklore thunderstones held strong magical powers that guarded against evil; they were thought to be candlesticks used by supernatural creatures called vättar that live under the floorboards and cause trouble if the house isn’t kept tidy (in some versions of the story they are distant relatives of Santa Claus). In eighteenth-century England, fossil belemnites were ground down and used as an ointment for horses with sore eyes. In Scotland, the traditional name for them was botstone; people would drop one in a horse’s water trough to treat a case of worms.
Bountiful fossil ammonites have also been put to practical use. In Victorian Britain, they were dug up and used to make the world’s first artificial fertiliser. As urban populations grew and more mouths needed feeding, scientists discovered that phosphate was a key ingredient for growing better crops. Expensive bird droppings, rich in phosphate and known as guano, were imported from Peru at substantial cost. Animal bones from knacker’s yards, shavings from bone-handled knife factories, mummified Egyptian cats and allegedly even human remains from European battlefields were all ground down and sprinkled onto arable fields. Then a source of phosphate was found much closer to home. Buried deposits of fossilised bones, mixed in with assortments of ancient animal teeth, claws, shells and the droppings of extinct marine reptiles were found to be an excellent source of phosphate. The concoctions came to be known as coprolites, from Greek words for dung and stone, even though only some of it was actually petrified poo; everything else technically should be referred to as pseudo-coprolites or better still, phosphatic nodules. In the mix were ammonites; after they died, the calcium carbonate in their shells was replaced with calcium phosphate from seawater.
A shallow Cretaceous sea that used to cover south-east England winnowed fossil ammonites from older rocks and swept them into dense piles. It was these ancient relics that triggered a coprolite mining rush and saw open-cast mines appear across the country. Great fortunes were made in digging up and processing coprolites, in particular around the city of Cambridge, where almost all of Britain’s raw phosphate came from.
The Sedgwick Museum of Earth Sciences in Cambridge has display cases filled with coprolites. Many of them were found by Harry Seeley, an assistant to Cambridge’s professor of geology in the mid-nineteenth century, Adam Sedgwick. Throughout the 1860s, Seeley paid regular visits to the nearby coprolite pits where he picked through the washing tanks to see what interesting and unusual specimens were turning up. On display today at the museum are grey and black ammonites, as well as bivalves and gastropods.
Besides the few specimens liberated by Seeley, estimates suggest another two million tonnes of phosphate-rich fossils were dug up and loaded onto horse-drawn carts, steam trains and barges and taken away to be crushed in windmills. Sulphuric acid was then added to the powder to make ‘superphosphate’, which was sold for half the price of Peruvian bird droppings and was exported across the globe. Until cheaper sources of rock phosphate were found in the 1880s and coprolite production fell, arable crops from Russia to Australia were grown with the aid of some very old seashells.
Fossil ammonites have left another, more lasting legacy in the human world. Two hundred years ago, British engineer William Smith was the first person to realise that fossils, and in particular ammonites, were time capsules that declare the age of rocks. His job involved travelling the country, digging a new network of canals. He noticed that as his men dug deeper the rocks changed, and so did the fossils inside them. He gathered together a fine collection of fossils, including many ammonites, and used them to prove that rocks are deposited in flat layers like pancakes; later those flat rocks can become squashed, tilted and folded as the Earth’s crust shifts.
Several features of ammonites made them extremely useful to Smith as he probed geological formations. Not only were their fossils immensely abundant and easy to find, but there were also thousands of ammonite species (many can be identified from intricate patterns like fingerprints, called sutures, etched across their fossilised shells; these were the junctions between the internal chamber walls and outer shell, with the lines revealed when sand and mud filled an empty shell, then formed an internal mould). Individual species also tended to be quite short-lived, appearing and then going extinct in a geological heartbeat, sometimes just a few hundred thousand years. This means that if the same ammonite species is found in different locations, the rocks they lie in must be roughly the same age. This is the basis of a powerful geological technique known as biostratigraphy. With their cosmopolitan ranges, ammonites assist geologists in linking rock formations on opposite sides of the planet. The same species have been found in Chile, Australia, Europe, Madagascar, China and Antarctica.
By matching the ages and types of rocks in different places, Smith drew an enormous map, two metres (more than six feet) tall, showing in fine detail the geology of England, Wales and part of Scotland. With different colours for different rock formations, he produced a rainbow view of the British Isles that had never been seen before. The map and Smith’s findings played an important part in the emerging science of geology, helping to advance theories of how rocks are formed over millions of years.
You say ammonite, I say ammonoid
A confusing thing about ammonites is that, technically, rather a lot of them should in fact be referred to as something else. The lineage that ammonites belong to – the ammonoids – split from the rest of the cephalopods in the Devonian around 400 million years ago. The true ammonites showed up more than 200 million years later, in the Early Jurassic. Before then, dozens of other ammonoid groups came and went. People usually refer to them all as ammonites, but in fact they were different, closely related animals.
In Palaeozoic seas, from the Devonian onwards, the dominant ammonoids were the goniatites, most of them with small, compact spiralling shells. They thrived until 252 million years ago when a crisis hit the living planet, one like none that had come before. The End-Permian mass extinction, also known as the ‘great dying’, was probably triggered by a combination of colossal volcanic eruptions, the bubbling up of methane from the deep sea and subsequent runaway global warming. It wiped out 70 per cent of life on land and 96 per cent of ocean-going species, including the last of the trilobites. Even though the goniatites went extinct, the ammonoid lineage survived into the Triassic. The oceans filled with the next major ammonoid group, the ceratites. They were quite short-lived, with a reign that lasted only 50 million years or so. Then one final, grand assembly of ammonoids took centre stage. From the early Jurassic onwards, the oceans were teeming with ammonites.
Even though their fossils are incredibly abundant, the ammonites and their relatives remain deeply mysterious creatures, and many of their secrets remain locked in the past. Apart from their shells, we don’t know what ammonites looked like. So far, not a single fossil ammonite has been found with its soft body preserved. Did they have eight arms like octopuses? Eight arms and two tentacles like squid and cuttlefish? Or did they have dozens of noodly appendages like nautiluses? We don’t know.
One thing we do know is that they probably swam around by jet propulsion. A notch in the opening of ammonite shells hints that they had a fleshy funnel, like living cephalopods. It’s mind-numbing to imagine the biggest known ammonite, Parapuzosia, pulsing its way through the seas – fossils of their shells are two metres (six and a half feet) in diameter. Experts think the living creature could have been three metres across, and weighed a tonne and a half or more. If giants drove around in monster trucks, these shells would be their wheels.
There were plenty of other strange sights in the oceans during the reign of the ammonites. On the whole, their shells were sculpted into neat spirals; they occupy just a small corner of David Raup’s museum of all possible shells. Some ammonites, though, did things completely differently.
Helioceras was an ammonite with a tall, helical shell covered in spikes that looked like a dangerous helter-skelter. They would have hung with their heads down, and a gentle puff of water from their funnel would have sent them into a spin. Perhaps they pirouetted up and down through the seas like corkscrews. Nipponites was another strange ammonite. It had a meandering shell, tangled up in knots, similar in appearance to (but much bigger than) the microsnails that live today in the chalk hills of Borneo.
Something else we don’t know about ammonites is what they ate. Rare fossils have been found with what could be their stomach contents, including little creeping crustaceans called ostracods and flower-like relatives of sea urchins called crinoids, as well as other ammonites. But not everyone agrees that these definitely were the ammonites’ last meals. What is clear, though, is that other animals were eating ammonites. They were not the highest-ranking predators in the oceans, as their Ordovician ancestors were. The hunters had evolved into the hunted.
Fossil ammonites have been found with smooth, round holes in them and some experts think these are scars left by limpets that latched on after the ammonites died. Further analyses, however, point towards a more brutal endgame.
Jurassic ammonites shared the oceans with plenty of scary beasts, including dolphin-like reptiles, the ichthyosaurs, followed later by mosasaurs. These were terrifying marine lizards, up to 20 metres (65 feet) long with huge snapping jaws packed with teeth that just happen to match the size and spacing of the holes in many ammonite shells. Rather than limpet scars, a more likely explanation is that the holes are indeed tooth-marks. There seems to be no obvious reason why limpets would line themselves up, time and again, into the same V-shaped arrangements.
One ammonite has been found with punctures in two sizes: a perfect fit for adult and juvenile mosasaur teeth. Was an adult mosasaur teaching its offspring how to hunt? Or did it sneak up on a youngster and steal its dinner? Either way, it wasn’t good news for the ammonite.
Meanwhile, as giant swimming reptiles were chasing after ammonites, new threats to everything in the oceans were approaching. Soon the reign of the shelled cephalopods would come to an end, leaving one final, big question: why are there no ammonites around today?
Ammonites well and truly hogged the cephalopod limelight throughout the Mesozoic. Meanwhile, in the background, another group of shelled cephalopods were quietly getting on with things. These were the nautilids. From the outside, they looked a lot like ammonites but compared with their more famous cousins, they lived in much smaller populations and there were not nearly as many species.
Side by side, the ammonites and the nautilids survived multiple mass extinction events, and kept going until 65.5 million years ago. Then, at the end of the Cretaceous, a mass extinction came along that only one of these two groups would survive.
This is probably the most famous mass extinction of all, because on land it saw the end of the non-avian dinosaurs. It also hit the oceans hard: only one in five marine species pulled through into the Tertiary, and I certainly would have put my money on ammonites being among the survivors, rather than nautilids. There were far more of them, and they were more widespread, two factors that normally create a buffer against extinction. Even so, it was the ammonites that bade farewell to the planet while the nautilids persisted, giving rise eventually to the chambered nautiluses. And for a long time, palaeontologists have wondered why.
To pin down the causes of extinction is difficult enough in the present day. Even when biologists can tiptoe up to endangered species, watch them and test out ideas of why they are in trouble, it can still be a great challenge to decipher the real issues (and even harder to do something about them). Imagine, then, how much more difficult it is when the species in question are already long gone, leaving behind only traces of themselves in rocks. All we have are theories. Researchers have scrutinised the ammonites, then the nautilids and details of the mass extinction, hunting for explanations of what happened and what went wrong for the ammonites.
The longest standing theories about why ammonites lost out are linked to the way they are born. Hatchling ammonites, known as ammonitella, were tiny. We know this because, if you look carefully, you can see the smooth, inner whorls of a fossilised ammonite shell that grew in predictable conditions while it was still inside its egg, feeding off yolk. As soon as it hatched and had to fend for itself in the erratic outside world, new shell layers became irregular. For ammonites, those uneven whorls began to appear when the shell was only one millimetre across. Young nautilids, on the other hand, were around ten times bigger when they hatched. It’s thought that at a tender age, these two groups were doing very different things. Ammonites were drifting through the water, as part of the plankton, while nautilids probably stuck closer to the seabed.
This difference may not have mattered too much when the going was good, but it could have been the downfall of ammonites when things got stressful. The exact cause of this game-changing mass extinction is still hotly debated. The fossil record shows that leading up to it, the great ammonite lineage was already in decline, with many genera going extinct. Falling sea levels, which dropped by as much as 150 metres (500 feet) in one million years, may have had something to do with it.
Then, the infamous asteroid, Chicxulub, slammed into Mexico’s Yucatán Peninsula, casting dust clouds across the Earth and triggering a long, dark winter. Many experts think this alone explains the extinctions, while others argue that massive volcanic activity in India also had its part to play in the downfall of life on Earth. Today, the Deccan Traps in central India consist of a layer of solid basalt, two kilometres deep and half a million square kilometres in area, which gives an idea of just how enormous these volcanic eruptions and lava flows were. They would have spewed carbon dioxide and sulphur dioxide into the atmosphere, contributing to the planet-wide changes.
Sulphurous gases in the atmosphere would have combined with water and fallen in showers of acid rain; this would have turned shallow seas more acidic and could have made life distinctly uncomfortable for planktonic species, including young ammonites, floating around inside chalky skeletons. By contrast, the next generation of nautilids were tucked up safely down in the deep sea, out of reach of the worst effects of these corrosive waters.
Diet may also have had a part to play in the ammonites’ demise. In 2011, Isabelle Kruta and colleagues conducted a detailed three-dimensional scan of an ammonite called Baculites. She found what she thinks are remains of its last meal, including the planktonic shell of a gastropod larva. Other experts contend that we can’t be sure if this plankton really was food or just a passer-by that got caught in the same rock. But if ammonites did have a microscopic diet, then a collapse of planktonic populations – triggered by corrosive, warming waters during the extinction event – could have left adult ammonites starving.
As for the nautilid diet, their living descendants provide clues as to what they ate. During the day, chambered nautiluses stay hundreds of metres beneath the waves, then rise up at night into shallow coral reefs where they scavenge for the dead. And being seriously short-sighted, chambered nautiluses sniff rather than see their food. They have a pair of sensitive pits, called rhinophores, that help them pick up the whiff of a decomposing body from at least 10 metres (33 feet) away and track the odour plume in three dimensions through the water; scale that ability up to a human standing at the starting blocks of a 100-metre running track, and they could sniff a ripe Brie sandwich being eaten at the finish line. Ancient nautilids may have had a similar habit of smelling and groping their way towards dead food scraps, and it could have made them more resilient to changes in the water around them. Down in the deep, there would have still been plenty to nourish animals that weren’t too fussy about their food.
Recently, a new piece was added to the ammonite puzzle when Neil Landman, from the American Museum of Natural History in New York, pondered the importance of geography. He mapped out the global distribution of ammonites that lived towards the end of the Cretaceous, including a handful that survived the mass extinction – for a while, at least. The species that were swiftly snuffed out were ones that had relatively small ranges. By the same token, ammonites that hung on for a while longer generally occupied a wider sweep of the planet. It makes sense that species with smaller ranges are often more vulnerable to extinction. They have all their eggs in one basket, geographically speaking, and are more likely to get wiped out in one go, perhaps by a random event. Imagine a species of dung-eating insect living only in a single cowpat, and what happens if a cow happens to tread on that very turd.
Landman and his colleagues put their findings forward as good evidence that ammonites with a wider range were initially protected, although in the long run it was no guarantee of survival. Ultimately, all the ammonites went extinct (and no palaeontologist truly believes that ammonites could still be out there, somewhere, hiding in the deep). The dying ammonites left the nautilids alone to continue the ancestral line of shelled cephalopods, after almost 400 million years in the sea.
Having followed the rise and fall of the ammonites, let’s return to the question of ammonites and argonauts. Could argonauts have learned their shell-making skills from these long-lost ancestors? Nice idea, but there is a fundamental flaw – ammonites and argonauts probably didn’t exist at the same time.
We know of 10 extinct argonaut species from the fossilised remains of their delicate shells. The oldest is Obinautilus from the Oligocene around 29 million years ago, although some palaeontologists consider this to be a nautilid, which leaves the oldest fossil argonaut at a youthful 12 million years old. Meanwhile, the last known ammonites, as we’ve just seen, went extinct shortly after the mass extinction at the end of the Cretaceous, around 65 million years ago. More fossils could still be found to fill this gap but, as things stand, it looks highly likely that argonauts never actually encountered any living ammonites, let alone began copying their shells, and it’s now widely agreed that this almost certainly didn’t happen.
There really is only one plausible explanation for why argonauts have shells that resemble extinct ammonites: it is simply a striking case of convergent evolution. They look so alike because each evolved under the same selective pressure – to be streamlined underwater. Studies have shown that the ridges and ribs on argonaut shells reduce drag while they swim through water, stabilising them and limiting the amount they rock from side to side while they propel themselves along. The same thing would have applied to ammonites too, all those millions of years ago.
Even if argonauts didn’t model their shells on ammonites, the question of whether they parasitise some other creatures or make their own shells still needed to be answered. Back in the nineteenth century, argonauts commanded a huge amount of attention and discussion. Scores of scientific papers were written. A few rare preserved specimens of shells with their baffling occupants were passed around. Lord Byron even wrote about them in his poem The Island. A host of illustrious scientists held strong views on the argonaut debate, with Richard Owen, Jean-Baptiste Lamarck, Joseph Banks and Georges Cuvier among them. Not everybody was taken in by the stories of octopuses sailing around in stolen boats, and many argued that Argonauta and Ocythoe should be united as a single species, shell and shell-maker in one. Italian naturalist Giuseppe Saverio Poli examined young octopuses under a microscope and saw they were encased in a little shell, thus proving – he was convinced – that they were not parasites.
In the end, the issue was resolved by a now largely forgotten pioneer of marine biology, who devoted herself through the 1830s to uncovering the truth about these strange animals. Her story of the argonauts follows a meandering journey, taking in a princess’s wedding dress and a groundbreaking piece of technology along the way, and ending in the solution to the contentious puzzle of how the argonaut got its shell.
The lady and the argonauts
Jeanne Villepreux was born in 1794, a long way from the sea. She grew up in Juillac, a village in rural south-west France, the eldest child of Jeanne and Pierre. Not a lot is known about her upbringing, but her family seemed to be reasonably well off. Jeanne’s father was noted in local records as a shoemaker, shopkeeper, landlord and Juillac’s first policeman. When Jeanne was eleven her mother died, and her father remarried. It’s not known how well Jeanne got on with her step-mother, who was half her father’s age, but she stayed at home until she was 17 before setting off for a new life in Paris.
Chaperoned by her cousin and a herd of cows, Jeanne walked almost 300 miles to the capital. It should have taken around two weeks but the journey was interrupted, so it seems, when her cousin assaulted her and Jeanne sought refuge in a convent in Orléans. She finally made it to Paris and began a job as a seamstress, something she was clearly very good at because it wasn’t long before she took part in a royal wedding.
Jeanne was entrusted with embroidering the wedding dress of an Italian princess, Marie-Caroline, the Duchess of Berry, for her marriage to Charles Ferdinand D’Artois, a nephew of King Louis XVIII.
Among the congregation of French and Italian dignitaries was James Power, originally from the British Caribbean colony of Dominica, who had become a wealthy merchant based in Sicily. In 1818, two years after meeting at the royal wedding, Jeanne and James were married in Sicily. The couple settled in Messina, a port on the east coast, where Jeanne became a lady of leisure. She no longer sewed or embroidered dresses for a living, and she didn’t continue with such genteel pursuits to keep herself busy, as most other aristocratic ladies were expected to do. Instead she rolled up her sleeves and became a scientist.
On Jeanne’s doorstep was the Strait of Messina, the narrow gap between Sicily and the Italian mainland that connects the Ionian and Tyrrhenian seas. For mariners this is a dangerous place where ferocious currents race north and south, switching direction every six hours and sucking tides swiftly up and down. Much feared since classical times, the strait’s raging whirlpools and rocky reefs were personified as two sea monsters in Greek mythology, Scylla and Charybdis.
The six-headed shark-toothed beast, Scylla, guards one side of the strait. In Homer’s epic poem The Odyssey, the hero Odysseus narrowly escapes being devoured by Scylla, although several of his companions aren’t so lucky. In a later encounter, Odysseus drifts back through the strait on a raft and this time gets a bit too close to Charybdis, the whirlpool, who sucks up masses of water into her enormous mouth along with the unfortunate Odysseus; he clings on to his raft and waits until Charybdis belches him back out, spinning whirlpools across the sea. In another ancient story, Jason and his crew of Argonauts sail through the perilous waters between Scylla and Charybdis on their way back from stealing the Golden Fleece. They only survive their encounter because Jason convinces Thetis, a sea nymph, to guide the way.
When Jeanne arrived in Messina and began pondering the legendary strait, she didn’t go hunting for menacing beasts such as Scylla or Charybdis. Instead she became entranced by some of the real creatures that inhabit these turbulent waters.
Jeanne’s interests in the natural world had already begun to lead her around the island, which she would explore for the next 20 years. She wrote a guidebook to the island’s wildlife, and studied caterpillars and butterflies, starfish, crabs and even Noble Pen Shells; she described watching an octopus wedging a stone between the pinna’s twinned shells before devouring the mollusc inside. Way ahead of her time, she came up with the idea of restocking overfished rivers with fish and crayfish. She also tamed a pair of pine martens that lived in her house while she observed their behaviour; she brought a tree inside for them to climb in, and live birds and squirrels for them to hunt. And it was a curious marine species that tempted her to embark on a revolutionary study. Jeanne realised that she was in the perfect place to answer a time-worn question: do argonauts borrow, steal or make their shells? She knew that to find an answer she had to do something no one else was doing. She would spend a lot of time with living argonauts.
Jeanne had a ready supply of these animals from the seas around Sicily; fishermen sometimes snagged argonauts in their nets and gave them to her, and she also ventured out and caught them herself. All she needed was a way of keeping them alive while she observed and experimented with them, so she devised a series of brand new observation platforms.
One was a simple box, later dubbed the ‘power cage’: four metres (thirteen feet) wide, two metres (six feet) tall and a metre (three feet) deep, with a door that flipped open on top and two glass observation windows so she could peer in. At each corner was a small anchor that fixed the contraption to the seabed at the shoreline. The cage walls were made of narrowly spaced bars that kept a fresh supply of seawater flowing through, but held the argonauts and their shells captive inside. Jeanne also built a glass tank in her house. It was the world’s first aquarium. Her inventions let Jeanne observe the marine world in a way that no one had ever done before, and she settled in for months and years of patient observation and learning.
Watching adult argonauts swim around her aquariums, she saw how easily they climbed all the way out of their shells, and how they aren’t permanently fixed inside like all the other molluscs with shells, including the chambered nautilus. She saw how the argonauts held on to the shells with their suckered arms, and noted that they never abandoned their shells altogether.
This was one of the pieces of accurate biology that Jules Verne included in Twenty Thousand Leagues Under the Sea. Professor Aronnax tells his servant, Conseil, about argonauts never choosing to leave their shells, even though they’re free to go at any time. In reply, Conseil remarks that Captain Nemo should have called his ship not the Nautilus but the Argonaut, because he too could leave, but chooses to stay confined inside.
Argonauts were clearly different from the other cephalopods Jeanne studied. Placing common octopuses inside her aquarium, they swiftly munched any food on offer before slipping their soft, unshelled bodies through the bars and slinking off into the open sea. This was something the argonauts never did, choosing to hang on to their shells and remain stuck behind bars. And when Jeanne took away their papery spirals, the argonauts died. She concluded that if they were borrowing shells from other animals, then surely they would have wandered outside the cage to try to find another one.
Fracturing their shells and leaving them in place, Jeanne saw that even though argonauts can’t make new shells, they do know how to a mend a broken one. Her injured argonauts rubbed the surface of their shells with silvery, web-like membranes at the end of two of their arms, which exuded a sticky substance that sealed up the cracks. Analysing the glue’s chemical make-up, Jeanne matched it to the calcium carbonate of the original shell.
Next, she tried breaking off small chunks of shell. After being inflicted with this new level of damage, an argonaut would spend hours sorting through bits and pieces on the aquarium floor, testing out shell fragments to find ones that were a perfect fit for the gaps; it would then glue the chosen pieces in place on its shell to complete the broken jigsaw puzzle.
The discovery that argonauts are equipped with these expert shell-fixing skills lent more support to Jeanne’s argument that they do indeed make their own shells and don’t simply steal them from other animals. But there was still one final part of the picture left to find: Jeanne needed to catch an argonaut in the act of actually making a shell.
Contrary to the reports made by Giuseppe Saverio Poli, Jeanne saw no sign of a shell when she examined unhatched argonaut eggs. However, she carefully watched as they hatched and grew up, and saw that when the young animals reached the size of a little fingernail, around nine millimetres (a third of an inch) across, they began to build their hard outer covering. As the argonauts got bigger, so did their shells.
Thanks to Jeanne’s extensive research, there was no longer any doubt that argonauts do indeed make their own shells, and that they do it in a completely different way from all the other molluscs. Instead of secreting a shell with their mantle, argonauts have shell-making glands at the end of those two arms that she observed repairing breakages; these are spread out into broad membranes (the very same ‘sails’ that Aristotle imagined argonauts unfurled to propel themselves over the seas).
All of these discoveries could have been lost and forgotten had Jeanne not kept up with her correspondence, and been good at publishing her findings. When Jeanne and James Power decided to leave Sicily and live in London, then Paris, they travelled overland. Meanwhile Jeanne arranged for the bulk of her papers and research equipment to be sent on afterwards by sea; everything was packed up and loaded onto a sailing ship bound for London. A short way into the voyage, off the French coast, disaster struck. The ship sailed into a storm and sank, sending Jeanne’s treasured collections into the ocean depths (the kind of romanticised disaster that rarely strikes scientists today, but perhaps a reminder to do regular data backups – the modern equivalent of avoiding a shipwreck).
Jeanne’s findings live on in pages of letters she wrote to Richard Owen at London’s Natural History Museum, and in the various papers and studies presented in scientific journals. However, her legacy as an early female scientist has faded and she is little remembered for her achievements. Her dedicated research saw her elected as a rare female member of many scientific institutions in Italy, France, Belgium and England, including a corresponding member of the Zoological Society of London. Few people nowadays have heard of the lady who spent years watching, probing and asking questions about this obscure but captivating group of animals.
In the years since Jeanne Power conducted her studies in Sicily, knowledge of argonauts and their way of life has continued to grow. We know they feed on various other animals that live up in the water column, including fish, jellyfish and sea butterflies; we know the females make their shells by laying down material on the inside and outside; we know that no two argonaut shells are exactly the same because of the way they patch them up (this makes it extremely difficult to identify species based on their shells alone); we know that when argonauts meet they sometimes cling to each other and form rafts. No one really knows why they do this, but it could explain why hundreds of them sometimes strand together on beaches.
We also know a lot more about the argonauts’ strange sex lives. Throughout her studies, Jeanne noted that she only ever found egg-producing female argonauts. Where were the sperm-making males? She was the first scientist to suggest that the worm-like objects found stuck to female argonauts could be something to do with the males. When Georges Cuvier originally spotted this peculiar appendage he identified it as a parasitic worm, and in 1829 named it Hectocotylus. Much later, following Jeanne’s suspicions, it transpired that these were not in fact worms at all but important mementos left behind by inconspicuous males.
Without doubt the less impressive of the sexes, male argonauts can be 12 times smaller and weigh 600 times less than females; they barely reach the size of a peanut. The males don’t make shells, but they do have an impressive trick up their sleeves. One of their eight arms is specially modified into a sperm-delivery organ. In other words, they have a penis on the end of an arm. What’s more, the male argonaut’s penis is detachable.
The word hectocotylus is now used for the arms of many male octopuses and squid that dole out packets of sperm to females. Amid a grabby clinch of arms and tentacles, the male will reach into the female’s body (in argonauts there is a cavity under the mantle; in other octopuses the male pokes into the female’s body just under her eyes). He detaches his wriggling, sperm-laden limb, which clamps on to her with suckers. Female argonauts will often collect and carry around the offerings from several males at once.
After dropping their penis some male cephalopods will grow a new one, but not male argonauts. They only get one shot. Their arm drops off, hopefully stuck to a receptive female, and shortly afterwards they die. Female argonauts, on the other hand, keep going and unlike their octopus cousins they can rear many clutches of young over the course of their lifetimes. Most mother octopuses deposit their eggs inside caves and crevices on the seabed. They will usually stick around to watch over their offspring, to fend off predators and keep their broods well oxygenated with wafts of clean water. A deep sea octopus has recently been seen in the Monterey Canyon off the Californian coast guarding her eggs for 53 months, by far the longest period of egg-brooding ever seen in any animal. After all that time, and possibly even longer, she will most probably die, as most female octopuses do, after their single, tremendous reproductive effort.
Living up in open water, where there are no caves to lay their eggs, female argonauts make their own portable, protective nooks to nurture their young. But their shells aren’t just brood chambers, they do other things besides. Watching argonauts for brief periods in aquariums, some scientists have argued that air trapped inside their shells is nothing but a nuisance, making it difficult to steer and stranding the animals at the water surface. Others have entertained the possibility that argonauts wilfully manipulate air bubbles inside their shells, and use them like underwater blimps.
It wasn’t until 2010 that this matter was put to rest, when Julian Finn from Museum Victoria in Melbourne, Australia paid a visit to the Sea of Japan. Three female argonauts were caught in fishing nets offshore and brought into Okidomari Harbour, where Julian climbed into his scuba gear and carefully took the argonauts with him down beneath the waves. He emptied all the air out of their shells and released them, one at a time, and watched while all of the argonauts performed the exact same routine.
First the argonauts zipped straight upwards, squirting themselves along using jet propulsion. Arriving at the surface, they squeezed out an especially vigorous jet of water that let them bob up and draw as much air into their shells as possible. Next, the argonauts repositioned their funnels and jetted back down, pushing themselves deeper and deeper. Being essentially open to the water and not fully sealed off, the air bubbles inside their shells were squashed, and shrank as the argonauts swam down and the pressure around them increased. Eventually the argonauts reached a depth where the air volume inside their shells cancelled its weight and the animals became neutrally buoyant, and therefore effectively weightless: they didn’t sink or float but hovered in the water column. On reaching that magic depth, between seven and eight metres (about 25 feet) down, the argonauts scooted off horizontally at high speed, swiftly outswimming Julian and his diving assistants.
Watching them disappear from sight, Julian was certain that the argonauts were deliberately using air as a tool to help them swim efficiently at a shallow depth beneath the sea surface, where they are less likely to get knocked around by waves or picked off by a hungry seabird from above. It would explain why the exhausted argonaut brought to the Cabrillo Marine Aquarium needed a helping hand to fill up her shell at the surface and gain some much-needed buoyancy.
Modern genetic studies confirm that the paper and chambered nautiluses are only distant cousins. Argonauts are without doubt octopuses, members of the coleoid lineage alongside cuttlefish and squid. And the nautiluses are the last few survivors of an ancient cephalopod pedigree, the nautilids, that have been doing their own thing for more than 400 million years.
After all that time, these two groups of animals are living proof that having a gas-filled shell is an efficient way of moving through the oceans. They may not be as agile and swift as some of their cephalopod relations, but they are certainly not as primitive or outdated as the label ‘living fossil’ implies. And we now know for sure that when nautiluses die and leave their shells behind, argonauts don’t pick them up and use them.
But humans do.