Australasian Science: Australia's authority on science since 1938

Sinking Aristotle’s Sailing Octopus

argonaut

A female argonaut (Argonauta argo) swimming close to the sea surface in the Sea of Japan. Photo: Julian Finn, Museum Victoria

By Julian Finn

By expertly manipulating air gathered from the sea surface, argonauts are able to control their buoyancy and traverse the world’s oceans at depth.

In 300 BC, Aristotle wrote of a peculiar octopus that rises from the deep to sail on the ocean surface in a boat made of shell. Using two arms as sails and six arms as oars, it was said to have navigated the oceans of the world.

Two thousand years later, we now know that Aristotle’s fanciful octopus was in fact the pelagic octopus, named Argonauta by Linnaeus in 1758 on account of this sailing reputation. The boat, as Aristotle referred to it, is the beautiful white shell of the female argonaut. The sails are specialised webs used for secreting this shell.

Argonaut shells have long been familiar to coastal communities. Their image adorns artefacts dating back to Minoan civilisations (3000–1050 BC).

Despite this long familiarity, the elusive nature of the argonaut has kept much of their lives a mystery, including the true function of their shells. Recent wild observations of live argonauts have revealed that the shell is a precise hydrostatic structure employed by the female argonaut to obtain and accurately regulate buoyancy at varied depths.

Argonauts (family Argonautidae) are pelagic octopuses that live their entire lives without touching the sea floor. Due to morphological and molecular similarities, it is believed that the ancestors of the argonauts were bottom-living octopuses that departed the sea floor to invade the open ocean.

Argonauts are renowned for their extreme sexual size dimorphism, with the females of some species growing up to eight times the length and 600 times the weight of the largest males.

Female argonauts are most widely recognised by their beautiful white, single-chambered shells. These shells, commonly known as “paper nautiluses”, are not true molluscan shells – they are produced only by the females using their arms (not their mantles) and are gripped by their suckers (not permanently bound to their bodies).

Argonaut shells also differ from the shells of other cephalopods, being constructed of calcite. This is a different form of calcium carbonate than aragonite, which makes up the shells of the chambered nautiluses (subclass Nautiloidea), ram’s horn squid (family Spirulidae) and cuttlefishes (family Sepiidae).

Female argonauts start building a shell when they are extremely small (less than 10 mm in total length), and continue adding to the shell as they grow. The largest shells exceed 300 mm in diameter.

By contrast, male argonauts are tiny dwarves, never growing larger than a few centimetres. Unlike female argonauts, males do not produce shells. Their entire reproductive output is loaded into a specialised arm that is severed and passed to a female in a single mating event.

Confusion has long surrounded the argonauts. Their extreme sexual dimorphism and bizarre mating strategy have perplexed naturalists for centuries.

In the early 1800s it was widely believed that the octopus commonly found in the argonaut shell was not the rightful owner, but a parasite having devoured the original occupant. The minute shell-less male remained a mystery until the mid-1800s, with its detached reproductive arm originally thought to be a worm and described as a parasite, then erroneously considered to be the entire male argonaut.

One confusing aspect of the argonauts’ lives that has persisted to the present is the role of air in the shells of female argonauts. Past observations of wild argonauts floating at the sea surface with air trapped in their shells were thought to be accidents of life near the sea surface. It was proposed that air inadvertently caught in the argonauts’ shells could ultimately trap them at the surface and result in their demise in mass beach strandings. Such mass strandings are occasionally reported from southern Australia, with thousands of argonauts washing up on beaches in single stranding events.

Observations of female argonauts in aquaria failed to resolve the situation. Captive female argonauts were reported to display varied degrees of buoyancy as a result of air trapped in their shells – from being upright on the substrate to being trapped at the water surface. These studies, however, were not able to determine the source of the air or whether it was obtained or regulated by the argonaut. Aquarium aeration devices were even considered as potential sources of the air within the argonaut shells. Despite a lack of supporting evidence, these studies were used to support the assumption that female argonauts attain neutral buoyancy by way of pockets of air in their shells – an assumption that subsequently gained popular acceptance in the literature.

While completing my doctoral research revising the world’s argonaut fauna, an opportunity arose to travel to Japan to investigate this dilemma. My objective was to collect wild argonauts and take them to a sheltered, controlled environment where I could observe, while SCUBA diving, their response to varied volumes of air within their shells.

Three live and uninjured female argonauts (Argonauta argo) were collected from a fishing enclosure in the Sea of Japan. The argonauts were immediately transported to a nearby cove for observation and manipulation.

Prior to initially releasing the argonauts underwater, great care was taken to ensure that no air was in the shells. This was achieved by holding the argonaut inverted underwater until any trapped air eventually bubbled out. Once completely depleted of air, the argonauts were released at depths of 2–3 metres below the water surface and their behaviour documented using underwater photography and video. To my delight, the argonauts immediately put to rest decades of conjecture regarding the role of air within their shells.

When released, each argonaut immediately performed the same five-step behavioural sequence.

1. The argonaut used jets of water directed through its funnel to swim towards the sea surface.

2. At the surface, the argonaut directed the funnel dorsally and vigorously jetted, causing the shell to bob above the surface and rock forward, “gulping” the maximum possible volume of air into the shell via the dorsal openings of the shell aperture. The captured air was then sealed within the shell using the flanged second arm pair.

3. The jetting funnel was then redirected ventrally, causing the shell to roll away from the water surface.

4. Using strong jets, the now-buoyant shell was forced downward.

5. The argonaut levelled out at a depth of about 5 metres, where the buoyancy from the trapped air volume (now compressed by the water pressure) cancelled the weight of the animal (i.e. where neutral buoyancy was attained). The neutrally buoyant argonaut was then capable of rapid horizontal movement, easily outswimming a diver.

The method by which the female argonauts capture and manage air is a complex, multi-stepped behavioural sequence. By rocking the shell at the surface and sealing off the air with the arms, the female argonaut is capable of capturing a larger volume of air than would be possible with a passive shell at the surface. This larger volume of air allows the argonaut to maximise the depth at which it attains neutral buoyancy, potentially reducing the impact of surface wave action and/or the risk of predation from above (e.g. from seabirds).

In all instances the released argonaut immediately targeted the acquisition of air. With no air bubbles within its shell, the argonaut appeared to have difficulty maintaining its vertical orientation and the shell would flail from side-to-side as the argonaut swam. However, once air was added to the shell the argonaut gained a stable vertical orientation, with the shell remaining upright during swimming.

At all stages, released argonauts had complete control of air within their shells, and consequently control of their buoyancy. Once the captured volume of air was sealed off by the argonaut in the shell, physical manipulation underwater, including complete 360° vertical rotation, resulted in no air loss.

Observations of argonauts in the wild were essential for resolving this behaviour. To attain neutral buoyancy the female argonaut must capture a large volume of air at the sea surface and force it to depth. At depth, the pressure of the water reduces the captured air’s volume, and consequently its buoyancy.

The female argonaut dives to a depth where the reduced buoyancy of the compressed air exactly cancels her body weight. At this point she becomes neutrally buoyant – she neither sinks nor floats.

Few aquariums offer sufficient depth for a captive argonaut to acquire neutral buoyancy. In the instance that the female argonaut cannot dive to sufficient depth to compress the captured air, she floats back to the water surface. It is quite likely that previous studies have failed to discover this behaviour because the argonauts were observed in aquaria that were too shallow.

Owing to superficial similarities in external shell shape, argonauts are often confused with their distant cephalopod relatives, the chambered or true nautiluses (subclass Nautiloidea). The live chambered nautilus is permanently bound to its solid shell, which is laid down by the mantle. The shell is internally divided to form gas-filled chambers connected by a long tissue duct (the siphuncle). The siphuncle functions to add and remove fluid from the chambers (using osmotic gradients) in order to attain the correct ratios of fluid and gas required for neutral buoyancy. Gas pressures within the chambered nautilus shell are less than one atmosphere, with the rigid shell preventing implosion and enabling these cephalopods to attain maximum depths of around 750 metres.

By contrast, the female argonaut is not permanently bound to its simple open shell. The argonaut’s surface-acquired air is subject to compression from water pressure, and hence the argonaut’s buoyancy varies with depths.

The argonaut’s buoyancy mechanism is potentially limited to depths less than 10 metres. Below this depth, water pressure compresses the acquired air to such a degree that it no longer provides sufficient buoyancy to counter the argonaut’s weight.

These distantly related cephalopod groups represent evolutionary convergence in the use of an external shell for gas-mediated buoyancy. For both groups, the selective advantages that led to their departure from the sea floor remain unknown. However, the dexterity and morphological plasticity of the female argonaut allows neutral buoyancy to be attained with far less architecture or complexity than that of the true nautiluses.

In the end, the argonaut shell proved to be more like Alexander the Great’s diving bell than Aristotle’s fantastic sailing boat.

Dr Julian Finn is a Curator of Marine Invertebrates at Museum Victoria. This study has been published in the Proceedings of the Royal Society of London, B: Biological Sciences.