Cephalopod molluscs, the group of animals that includes octopuses, nautiluses, bobtail squid and cuttlefish amongst its living members, is a small but highly diverse group of animals. The group boasts ocean giants, colour and shape changing octopuses, luminous ink squirters, transparent deep sea squid, aquarium escape artists, animals that mimic other animals, giant eyed vampire squid and they’ve even conquered the air in species that fly, yes fly (Muramatsu et al. 2013).

In short, it’s really hard to stand out at a cephalopod party without doing something really spectacular and yet there’s one group of octopods, the argonauts, which have a remarkable evolution on a par with the evolution of flight in vertebrates or the many groups like whales and dolphins which evolved from terrestrial ancestors to return to the ocean.

Argonauts, several species in the genus Argonauta, are a group of octopod cephalopods, the group that contains all the eight armed, soft bodied cephalopods. Collectively they’re known as octopuses but perhaps confusingly there’s a large number of species in the genus Octopus and many other genera of non-Octopus octopuses too such as Argonauta.

Argonauts get their name from the sailors of the Argo from “Jason and the Argonauts” fame. Nautilus also means sailor and it’s hypothesised that this was because argonauts were thought to sail on the wind using their webbed modified arms. I’ve not been able to substantiate if this was the case or if this is an apocryphal nineteenth-century re-imagining of an origin story.

There’s some debate about how many living species of argonauts there are, there’s a general consensus around four species but as many as 53 have been described (Sweeney and Young 2004). Argonauts have extreme sexual dimorphism, the males, for the species in which males have even been observed, can be as little as 4% the full length size of females and 1/600th the weight (Finn 2009). They carry their detachable sperm delivering arm in a sac under their left eye.

This alone makes argonauts somewhat remarkable amongst the cephalopods but what they are best known for is the calcite shell they make, which gives them the common name paper nautilus (although they aren’t closely related to true nautiluses which grow a hard outer shell). The delicate shell or case of argonauts have been washing up on shorelines for centuries puzzling naturalists as to who made them and how. Depictions of argonaut shells have been found in Minoan ceramics as far back as 3000 BC (Hughes-Brock 1999, Finn 2013). Initially it was thought that these were just the remnants of a shelled creature. When shells were found with cephalopods living inside them which weren’t attached to the shells, it was speculated that crafty octopuses had borrowed them from another creature much like hermit crabs appropriate gastropod shells to live in.

Shell of Argonauta hians. Photograph: Mark Carnall Photograph: Mark Carnall

It wasn’t until the nineteenth century, however, that Jeanne Villepreux-Power showed once and for all that argonauts create their own shells but not like other shelled molluscs. Females secrete the shells from modified arms and aren’t attached to the shells. They can be removed from the cases they make and they can patch up holes although experimentally they die when removed from the cases for prolonged periods of time. Males do not make these thin calcite shells although sometimes males are found loitering in the egg cases. Female argonauts form comedic awkwardly bobbing chains at the surface of the ocean and some species feed by spreading their modified web arms across the surface of their shells snatching food particl es that come into contact with them. They have also been found attached to jellyfish, chewing through the top of the bell to steal food from inside (Heeger et al. 1992).





Paper nautilus sighting off California. Video Dam Nguyen

If you’re lucky enough to find an argonaut shell not too damaged on the shore you’re looking at a form of octopus architecture. What makes argonaut shells amazing is that the shells are a flotation device which have allowed argonauts to return to the open ocean. It’s the cephalopod equivalent of humanity’s endeavour to venture into space and explore the stars.

I’ve mentioned previously that we don’t know a lot about octopuses from their limited fossil record but one ‘just so’ story about their evolution is that octopuses as a group lost their tentacles as an adaptation to living on the ocean floor (octopuses don’t have tentacles, the ten-armed squid, cuttlefish and bobtail squid do). Many octopuses are ranging foragers and ambush hunters adapted to navigating the sea floor in search of food, mates or a cosy den or two. By contrast the free swimming squid and cuttlefish rely on their lightning fast tentacles to ensnare fish, crabs and other invertebrates. If this simple hypothesis is correct then we can imagine ancient argonaut ancestors, sick of etching out a living on the ocean floor with a constant threat of predation from above looking to their squiddy cousins zipping about carefree in the open water and deciding to do something about it*.



So what does the fossil record tell us? Remarkably, there are fossil argonaut shells even though the odds are stacked against floating paper thin fragile shells preserving in the first place. Just over a dozen fossil species have been described. Two Obinautilus species are known from the Oligocene, 33-23 million years ago, and Miocene, 11-5 million years ago of Japan. Three other genera are known from the Miocene including two species of Mizuhobaris from North America, Kapal batavis from Sumatra and three species of Izumonauta from Japan and New Zealand. Several other species of Argonauta, the same genus as today’s living species are known from the fossil record. Two species we still have today, Argonauta hians and Argonauta argo are known from fossils from the Pliocene and Pleistocene respectively (Tomida et al. 2006).

Frustratingly, as is often the case with the fossil record, fossil argonaut shells strongly resemble the argonaut shells of today with the same pattern of ribs, nobs and tubercules offering little insight into how the argonauts evolved to float in the water column again. Looking at the close living relatives of argonauts - blanket octopuses, seven-arm octopuses (not the Pixar kind) and football octopuses (not the psychic kind) - there are some shared ecologies and behaviours but not the distinctive shells of the argonauts. Blanket octopuses (Tremoctopus spp.), football octopuses (Ocythoe tuberculata) and seven-arm octopuses (Haliphron atlanticus) are all pelagic (they live in the open ocean), have some degree of sexual dimorphism and all feed or interact with jellyfish and other gelatinous zooplankton. Blanket octopuses appear to be immune or resistant to Portugese man ‘o’ war stings and have even been observed wielding the stinging tentacles they’ve detached as a weapon. In addition blanket octopuses get their name from the long webs between their arms, perhaps a parallel evolution to the argonauts modified shell secreting arm? So it may be that argonauts were already pelagic octopuses before they evolved their characteristic shells.

Amazingly, it wasn’t until 2010 that scientists experimentally understood how argonauts use their shell constructions to float in the water column and control buoyancy. From observations of female argonauts released into water, argonauts jet to the water surface and bob their shells to gulp a pocket of air. Using their second pair of arms they trap the air in the top of the shell and dive releasing enough air to maintain the desired buoyancy (Finn and Norman 2010).

There are still so many questions that need answering when it comes to living argonauts. How do males find females? Why is it only the females that make and use shells? How and when did the argonauts evolve their remarkable shells and the complex behaviour that goes alongside maintaining the desired buoyancy? Sometimes the fossil record comes up short and it would be a pretty remarkable fossil discovery that would give us a concrete answer to all of these questions especially considering the low preservation potential of soft bodied animals and the presumably paper thin shell or proto shell we might hope to find. But then it’s questions like these that drive the work of scientists in the field and lab, perhaps more so than the answers we occasionally find.

*This is absolutely not how evolution works but it is a nice story.



References

Finn, J. K. 2009. Systematics and biology of the argonauts or ‘paper nautiluses’ (Cephalopoda: Argonautidae). PhD thesis, Department of Zoology, School of Life Sciences, Faculty of Science, Technology and Engineering, La Trobe University, Bundoora, Australia.

Finn, J.K. 2013. Taxonomy and biology of the argonauts (Cephalopoda: Argonautidae) with particular reference to Australian material, Molluscan Research, 33:3, 143-222

Finn, J. K and Norman, M. D. 2010. The argonaut shell: gas-mediated buoyancy control in a pelagic octopus. Proceedings of the Royal Society B.

Heeger et al. 1992. Predation on jellyfish by the cephalopod Argonauta argo. Marine Ecology Progress Series. Vol. 88: 293-296. Weblink here.

Hughes-Brock, H. 1999. Myceanaean beads: gender and social context. Oxford Journal of Archaeology 18, 277–296.



Muramatsu, K., Yamamoto, J., Abe, T. et al. 2013. Oceanic Squid do fly. Marine Biology. 160: 1171. Weblink here.

Sweeney, M.J. & Young, R.E. 2004. Taxa associated with the family Argonautidae Tryon, 1879. In: Tree of life web project. Weblink here.

Tomida, S., Shiba, M. & Nobuhara, T. 2006. First post-Miocene Argonauta from Japan, and its Palaeontological Significance. Cainozoic Research, 4(1-2), pp. 19-25.