The legend of the argonaut

A rare and misunderstood octopus, the argonaut lives far out to sea, where females construct fragile shells to live in, marble-sized males woo them with severed arms, and much of their lifecycle has never been observed.

Written by       Photographed by Paul Caiger, Irene Middleton and Crispin Middleton

The brittle, parchment-thin shells of adult female argonauts are often all that’s glimpsed of them in the wild. The shells are valuable enough among collectors that tracking strandings is difficult for scientists, with people often unwilling to disclose spots where shells may wash up in the future.

The outline of mainland New Zealand has long since receded from view. More than 30 kilometres out to sea, our boat gently drifts; the surface is glassy calm, the horizon an unbroken line encircling us. This is blue water, not the green of Northland’s coast. Beneath us, a clear oceanic current flowing south brings all kinds of life here from the tropics.

Irene and Crispin Middleton, photographers and fellow open-ocean explorers, settle in to wait for darkness. Irene checks her underwater camera rig, and Crispin makes some final adjustments to the lighting system to be deployed below the boat. Somewhere in the expanse around us, we hope, is an animal about the size of a human hand.

The odds are against us. In the ocean realm, life is spread far and wide. We’ve made dozens of expeditions over the past four years, by day and night, and we’ve found fully grown female argonauts only twice.

But we’re on a quest for argonauts exactly because they’re hard to find. Last summer, we came across just one, and that was enough to keep us returning to the depths.

First, we have to wait for the sun to set, and the waters to turn inky black. By day, the more vulnerable animals of the open ocean retreat to the depths to escape daylight predators. But the surface is where the food chain begins, triggered by sunlight—and so, each night, in the greatest migration on the planet, they rise to the surface to feed.

Slipping over the gunwale, accompanied only by a camera and lights, I fall into emptiness. My lights beam into the depths and I wait, watching for any flicker of movement or shimmer of colour, my senses on high alert. I can see another beam about 20 metres to my right—that’s Crispin—and behind me, the lights lowered beneath our boat to guide us back should we stray too far.

Around me, the water is alive. I’m surrounded, yet confined to a narrow field of vision. All manner of jelly-like animals drift by on the current, while flashes of blue in the darkness are bioluminescent organisms. Small red krill are drawn to me by the glow of the lights—little shrimps that swim with rhythmic pulses of their paddle-shaped legs.

Something frantic bumps my leg and I glance down to see a flash of white. It takes me a moment to realise I’ve found what I’m looking for—two pale shells bustling along, swimming with jerky, repetitive movements. Only their heads and eyes poke over the rim of their shells, and they fill their bodies and empty their siphons in rapid succession. Bobbing to and fro, they evade us with intermittent, propulsive jets of water and disappear into the black water.

Then we spot bubbles rising to the surface, and more little globes come into focus, jetting back and forth, their white shells lit starkly against the darkness. A score of argonauts, venting bubbles of air at the surface, some sheltering under the hull of our boat, others bumbling into our lights. It’s the first time we’ve seen more than a lone individual.

When I get up close to one, a pair of bulging eyes meets my gaze, peering over the edge of the shell, ready to retreat to safety at a moment’s notice.

I can see the outline of her body, and the vivid purple hue of her arms, tucked in alongside it—her shell is dimly pellucid, like sea-glass frosted by turbulence.

These fragile shells gave argonauts their name, and for a long time were their most mysterious feature. Argonauts are also known as paper nautiluses, but this is confusing, because they don’t belong to the nautilus family. They’re octopuses, a different order of cephalopod, and they’re pelagic—they live in the open ocean. Unlike their relatives, they never touch solid ground.

Why these octopuses have shells is a mystery that has perplexed people for millennia. Aristotle fantasised in his History of Animals, written in the fourth century BC, that argonauts stole their shells in order to use them as boats. To harness the wind, he said, they raised their two webbed arms above the surface as sails and used their remaining six arms to row. This notion stuck—both ‘nautilus’ and ‘argonaut’ mean ‘sailor’—for two thousand years or so. Then science spoiled the myth.

Argonauta nodosus is one of two argonaut species observed in New Zealand waters. Females fabricate shells as large as 25 centimetres in diameter, and tuck their arms inside—six of them long and tubular, and two of them short and wide, the ‘sails’ of legend. Meanwhile, males remain the size of a peanut, and don’t fabricate shells.

Argonauts don’t steal shells, they make them—females secrete calcite from the tips of their two webbed arms, the ones that Aristotle thought were sails. It’s the only animal in the world to produce a shell straight out of its arms.

While other octopuses usually lay eggs on solid ground, in the expanse of the open ocean, all the argonaut has is her shell, so thin as to be translucent. After depositing eggs inside, the female also shelters within, protecting herself and her young.

But the shell is more than a portable nest—it also provides a form of locomotion, allowing argonauts to control their position in the water column.

An argonaut sighted on the surface was long thought to have ended up there by mistake. Perhaps it had got air trapped in its shell and so could no longer descend, like a novice diver with no control over their buoyancy.

Museums Victoria senior curator Julian Finn set out to test this theory. He collected three females, released them in the safe confines of a harbour, and watched their behaviour. They immediately jetted to the surface, where they gulped in air, pivoted to shift it to the apex of their shells, and dove down to compress it. Then, by blocking or releasing the air pocket using their arms, they could precisely control their movements, the air acting as the equivalent of a modern-day buoyancy compensator.

Finn is the world’s only argonaut specialist—“I want to work on something no one else in the world works on,” he once told a group of cephalopod experts, and they said, without hesitating, “Argonauts”. As the sole authority, he spends a lot of time debunking myths.

Like the fact that there are only four species, no more, and though their shell is called a ‘shell’, that isn’t really the right name for it. It’s more of an egg case.

Female argonauts start building their shells straight away, as juveniles, and they never really stop.

A male argonaut clings to a chain of salps, small gelatinous filter feeders. His hectocotylus is stored in its sac, visible in this image as the opaque area above his funnel. The hectocotylus, which is severed and left attached to the female, was thought to be a parasitic worm until naturalist Jeanne Villepreux-Power identified it as a male organ in 1839. She was also the first to observe that argonauts made and repaired their shells, rather than stealing them.

“At about 12 days after hatching, when they’re about five to seven millimetres long, they’re already producing a shell,” says Finn. “At about 10 millimetres long, they’ve got a fully formed shell, and then she adds to that as she grows. If you look at the shell of one species, you can see a variation in shape—I think this is because she had to expand it quickly.”

If a shell is damaged, they repair it; if it’s lost, they make a new one. Sometimes the female is left with only a tiny fragment of her old shell, but she constructs a new one around it, incorporating the broken piece. After examining more than 1500 museum-specimen shells, Finn believes remade shells are sculpted differently from original ones, the difference arising from how rapidly they’re being made.

“I think if she remakes it, it’s really coarse and bumpy, and if she makes it as she grows, it’s fine.”

This variation in shell shape and sculpture has led to the identification of more than 50 argonaut ‘species’ when there are in fact only four, he says.

“I’ve got some shells which are half one ‘species’ and half the other—the variation is due to how the animal lives its life,” he says. “In the old days, people treated the argonaut shell like a mollusc shell—every different shell was a different species.”

Argonaut shells, though, are very different from mollusc shells—they’re made from a different material, they’re many-layered, and females aren’t attached to their shells, bound within them, as chambered nautiluses are; rather, they hold onto the shells with their suckers.

“In any other animal you would say it was an egg case. We don’t expect the same consistency from other structures made by animals to contain their eggs, but because this is called a shell, people expect it to be exact, and that’s where a lot of the confusion comes from.”

Another source of confusion has been the males of the species. Females are hard enough to find, but males are trickier—they don’t make shells, and they’re miniature.

Argonauts take sexual dimorphism to extremes: females grow up to 12 times the length and 600 times the weight of the males. In fact, the sexes look so dissimilar that the males were identified as the same species only about a century ago, while females have been part of science and folklore for thousands of years.

A juvenile female shelters beneath ocean detritus.

When we first saw the occasional tiny octopus, free-swimming far out to sea, we had to send photographs to cephalopod expert Steve O’Shea to confirm what they were. These were the males and juveniles we’d been looking for—marble-sized, roaming endlessly through space, occasionally hitchhiking on other marine life. On one dive, I saw a juvenile clinging to a mangrove seedling, and another time, a male catching a ride on the back of a buoyant jellyfish.

Males have a special arm called a hectocotylus, which stores sperm. It’s their third left arm, but they keep it in a pouch under their left eye. When a male is mature, he takes the arm out of the sac—it’s almost as big as his entire body—finds a female, severs the arm, and leaves it on her body. There, it crawls, with a life of its own, into her mantle.

“I’ve found female argonauts with up to 38 male arms in their body—this really popular female from Flinders Island—and they were all inside her mantle, wrapped around her gills,” says Finn. “From that I assumed that males are in schools, and occasionally, when they encounter females, they all give up their arms.”

The male, left with only seven arms, dies—no one has observed a male regrowing his arm—but his hectocotylus remains alive.

“After some time, male arms are still walking around— it’s bizarre, I don’t understand how they do it, but they can do it,” says Finn.

How long can the severed arm keep moving for? It’s one of the questions Steve O’Shea hopes to answer.

“Once when at sea, I’d removed a female from a trawl net, and placed her into a bucket of water containing a tranquilliser, several hectocotyli swam out and thrashed about for a good 10 minutes on the bottom of the bucket. They had a life of their own.”

This reproductive strategy is so bizarre that the males’ arms were long thought to be parasitic worms attacking the females, and after that, the arm was mistaken for the entire male.

Males may be one-shot wonders, but females can produce up to a million eggs in their lifetime, and some have been found with more than 100,000 eggs in their shells. That means there are probably a lot of argonauts out there, riding the currents and the wind, but the ocean is wide, and it’s not clear how often the fleets of males and females manage to find each other in that expanse. Finn suspects that encounters between the two are rare enough that males sever their arms at the first female they meet.

After young argonauts hatch—in their tens of thousands—what happens to them? It’s one of the octopus’s mysteries, says Julian Finn. “When they hatch, they’re tiny—among the smallest of all cephalopod paralarvae. They disperse into the water column, and we don’t know what happens next—where they go, how they survive.”

Observing them in the wild is a matter of luck, and holding them in captivity isn’t an option—female argonauts begin displaying signs of stress almost immediately.

“As soon as they’re placed in an aquarium, their ventilation goes up and they quickly deteriorate. They’re essentially dying; it’s just a matter of time. They’re used to being in the open ocean with no shadows around them. They just don’t confine well.”

Finn’s understanding of the argonaut lifecycle has been pieced together from chance encounters, from thousands of specimens he studied in museums around the world, from every anecdotal report he could glean.

There was a lot of information that simply hadn’t been assembled before, he says, but observations of behaviour are still few and far between.

“We don’t see these animals when they’re in their comfortable, natural environment, living their lives.”

Yet it’s thrilling to think that there are still discoveries to be made in the biology and behaviour of species in the wild—mysteries that remain for us to solve or speculate upon.

While the idea of the little octopus sailing the high seas, its arms raised aloft, turned out to be a fiction, there’s still plenty of delight in the notion of these strange sailors jostling to and fro beneath the surface in their translucent, homemade ships.