Scientists solve millennia-old mystery about the argonaut octopus

The argonauts are a group of octopuses unlike any other. The females secrete a thin, white, brittle shell called the paper nautilus. Nestled with their arms tucked inside this beautiful, translucent home, they drift through the open ocean while other octopus species crawl along the sea floor. The shell is often described as an egg-case, but octopus specialists Julian Finn and Mark Norman have discovered that it has another function – it’s an organic ballast tank.

An argonaut uses its shell to trap air from the surface and dives to a depth where the encased gas perfectly counteracts its own weight, allowing it to bob effortlessly without rising or sinking. Finn and Norman filmed and photographed live animals in the act of trapping their air bubbles, solving a mystery that has been debated for millennia.

Scientists have long wondered about the purpose of the argonaut’s paper nautilus. No less a thinker than Aristotle put forward a hypothesis. In 300 BC, he suggested that the female octopus uses its shell as a boat, floating on the ocean surface and using her tentacles as oars and sails. Despite a total lack of evidence for this ‘sailing hypothesis’, it was later championed thousands of years later by Jules Verne, who wrote about sailing argonauts in Twenty Thousand Leagues Under the Sea.

Since 1923 and the work of Adolf Naef, the shell has been viewed as a container for the argonaut’s eggs. After mating with a male (who is around 8 times smaller and 600 times lighter), the female secretes the papery shell using the tips of two large tentacles. She lays her eggs within the structure before snuggling inside herself. Besides her eggs, her only housemate is one of the male’s arms – the hectocotylus. The arm doubled as a penis, snapped off during sex and stays inside the female’s body.

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Besides the female, her eggs and her disembodied sperm package, the paper nautiluses often contain pockets of air. Naef viewed these as a problem. According to him, the unintended pockets eventually trap argonauts at the sea surface and cost them their lives. That would certainly explain the mass argonaut strandings that are sometimes found, but Naef didn’t have any evidence to back up his claims. Others have speculated that the air bubbles were caused by aeration devices in aquariums and are only seen in captive argonauts. Yet others have suggested that the animals deliberately use the air pockets to maintain their buoyancy but until now, that’s been mere speculation.

Into this debate came Finn and Norman. Their names may be familiar to regular readers – they have discovered the smash-hit octopus that carries coconut shells as a suit of armour, dolphin chefs that can prepare a cuttlefish meal, and the awesome mimic octopus. As with these earlier discoveries, their work on argonauts was based on observations of wild animals. They rescued three greater argonauts (Argonauta argo) from nets in the Sea of Japan, released them into Okidomari Harbour and filmed them as they adjusted to their freedom. It’s their beautiful video that graces the top of this post.

All of the females were checked before their release to make sure that they had no air already trapped in their shells. Without this air, they were in danger of sinking and had trouble keeping their shells upright. All three animals fixed this problem in the same way.

Each one used its their funnel to jet to the ocean surface and bob the top of its shell in the overlying air. The shell has a couple of apertures at the top, which allows the argonaut to gulp in air, sealing it inside with a quick flick of two of its arms. Having sealed away this pocket, it points its funnel upwards, rolling the shell away from the water surface and forcing itself downwards. At the depth where this compressed bubble cancels out its weight, the argonaut levels off and starts swimming.

Naef was clearly wrong. The air isn’t life-threatening or even unintended – the argonaut deliberately introduces it and has total control over it. Once the animals dived again, Finn and Norman grabbed them and rotated them through 360 degrees – not a single bubble emerged. “To my delight the argonauts immediately put to rest decades of conflicting opinions, demonstrating their expert ability at obtaining and managing surface-acquired air,” says Finn.

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This neutral buoyancy is a big boon for animals that live in the open ocean, because they don’t have to expend energy on keeping their place in the water column. Other cephalopods use a combination of fins, jets of water and, in the case of the actual nautilus, chambered shells. The argonauts are the only species known to use bubbles, but it’s clearly an efficient tactic. Finn and Norman observed that once they had trapped their air pockets and reached the right depth, they could swim fast enough to outpace a human diver.

By rocking at the surface, the argonaut can also trap a sizeable volume of air, which, in turn, allows it to reach a greater depth before becoming neutrally buoyant. Finn and Norman think that this may allow these unusual octopuses to avoid the surface layers of the ocean, where they would be vulnerable to birds and other top-level hunters.

This penchant for deeper waters may also explain why this behaviour has never been seen before, even though argonauts have featured in aquariums. They simply weren’t kept in tanks that were deep enough. The animals created air pockets as they would in the wild but without the ability to dive to the right depth, the air just brought them back to the surface again.

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As a buoyancy aid, the argonaut’s paper nautilus is superficially similar to the much harder shell of its namesake, the chambered nautiluses (right). These animals also use shells with trapped air, but theirs are permanently stuck to their bodies and divided internally into many gas-filled chambers. The two groups – nautiluses and argonauts – are only distant relatives, but they have both arrived at similar ways of controlling their buoyancy.

The argonaut’s solution is undoubtedly simpler and more flexible, but the nautilus’s sturdier shell prevents increasing water pressure from compressing the trapped air too much.  As a result, the nautilus can dive far deeper than the argonaut, to a depth of 750 metres.

Finn and Norman’s study may have solved a longstanding argonaut mystery but there’s still much to learn about these enigmatic and beautiful animals. Even though people have known about them since Ancient Greece, their behaviour, distribution and biology are still shrouded in secrecy. To find out more, Finn and Norman are conducting a survey reviewing Australia’s argonauts, and they’ve set up a website with details about how you could help them in their Argosearch.

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Reference: Proc Roy Soc B http://dx.doi.org/10.1098/rspb.2010.0155

Photos: Video and bottom photo by Yasushi Okumura, Japan Underwater Films; all other photos by Julian Finn

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