LAST August, I had the fortune to venture out to Osprey Reef, an isolated coral atoll 125 kilometres off the Great Barrier Reef. It is a wild and stunning place – a large reef system atop an extinct underwater volcano that rises precipitously from the sea floor more than 1000 metres below – but I wasn’t there for the scenery. The reason for my trip was to rejoin a research project I first got involved with nearly 40 years ago.
Osprey Reef is an excellent location to study chambered nautiluses, enigmatic but beautiful creatures that are related to octopuses, squids and the extinct ammonites. Nautiluses have long fascinated biologists because they are considered to be “living fossils” – species that have defied the evolutionary odds to survive virtually unchanged for tens or hundreds of millions of years. Like the coelacanths, horseshoe crabs, tuatara lizards, sharks and crocodiles, today’s nautiluses are all but indistinguishable from their distant fossilised ancestors.
Exactly why some species survive unchanged is not clear, but it seems there is a price to pay. Living fossils have a very low “evolutionary fecundity”: they may have lasted many millions of years, but at the same time they produce very few new species.
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For decades, nautiluses seemed to fit this bill, but new research into their evolutionary history and behaviour has produced an unexpected turnaround. Rather than being the last holdouts of a static lineage, the nautiluses appear to be in the midst of an evolutionary adventure, diverisifying at a rate that hasn’t been seen in their lineage since just after the extinction of the dinosaurs.
The nautiluses first appeared on the scene in dramatic fashion 500 million years ago. At that time, the animal world was entirely dominated by arthropods. A dive into the Cambrian sea would have been akin to swooping through the insect-filled air of a humid, tropical night – a zooming, crawling cornucopia of bugs. Whether predators, prey or scavengers, all the dominant animals were arthropods of one segment or another.
Then everything changed. A predator from a different phylum, the molluscs, arrived. These were the nautiluses, and they possessed a set of evolutionary innovations that made them by far the most formidable predators around, not least because of their superb manoeuvrability. Despite having heavy, impenetrable shells, nautiluses were somehow capable of making rapid darts and pinpoint turns, while also being able to hang motionless in the water, ready to drop on unsuspecting prey. Their secret was a shell lined with gas-filled chambers which gave them neutral buoyancy – the ability to stay suspended in water without sinking or rising.
They were also highly energetic, thanks to enormous gills and a new kind of blood pigment, the copper-based haemocyanin (oxygenated nautilus blood is blue). With all that oxygen coursing through their bodies, a new type of organ became possible: a large and probably calculating brain, certainly the highest level of intelligence seen in the animal world up to that point. Nautiluses also carried a lethal weapon – parrot-like jaws with cutting edges capable of slicing through arthropod exoskeletons. With the emergence of the nautiluses, arthropod evolution became a frantic race to develop armour, spines, larger bodies, improved eyesight and speed. Countless arthropods were gobbled up into the fossil record during this period.
For the next half-billion years, the nautiloid lineage flourished, surviving mass extinction after mass extinction. Their heyday was around 300 million years ago, when hundreds of species roamed the seas.
Today, though, only a handful remain. The exact number of species is disputed, but the Integrated Taxonomic Information System recognises just seven (see Map).
By rights the nautiluses should be extinct, yet they cling on. Not where they once ruled, in the food-rich shallows – nowadays they are more furtive, lurking by day deep in the shadows of coral reefs and stealthily rising at night to steal meals under the cover of darkness – but they’re still with us.
Scientific interest in nautiluses focuses on two main questions: their evolutionary history, and the workings of their exquisite chambered shells. The two are intricately linked, as the evolutionary breakthrough that elevated the nautiluses to top predator status was neutral buoyancy.
The buoyancy problem was cracked in the 1960s. The question was, how does gas gets into the chambers, especially as new chambers are walled off from the nautilus’s living quarters as its shell grows? To figure that out required the study of living specimens, but in those days no living nautilus had ever been brought to Europe or the US. So physiologists Eric Denton and John Gilpin Brown of the UK’s Marine Biological Association in Plymouth, Devon, travelled to the Loyalty Islands off New Caledonia in the south-west Pacific, where they succeeded in trapping and studying living specimens.
They eventually solved the buoyancy mystery, showing that newly-created chambers are originally filled with seawater which is removed by osmosis. First, salt ions are actively pumped out of the chamber, setting up an osmotic gradient with the nautilus’s blood. This gradient pulls water from the chamber into the siphuncle, a blood-filled tube-like structure that runs through the centre of the coiled shell, from where it is ejected into the sea. At the same time, gas – mainly nitrogen, oxygen and carbon dioxide – diffuses into the chamber from the siphuncle. Once filled with gas, a chamber generally stays that way, though small amounts of water can re-enter to allow fine tuning of buoyancy.
Having a chambered shell imposes strict limitations on the nautilus, however. The water pressure pushing in on the chambers is immense, and their shells are only capable of withstanding so much pressure. If they exceed a certain depth, they will fatally implode. For the modern nautiluses that depth is about 750 metres.
Even before they reach implosion depths, water pressure starts causing problems. Diving too deep causes the shell to start rapidly refilling with water, with potentially lethal results. In the 1980s, I did some experiments showing that the problems kick in at around 350 metres. Nautiluses kept in cages at 500 metres become so waterlogged that they can no longer swim. At that depth, water is forced into the chambers so rapidly that the osmotic emptying system cannot bail it out fast enough. Wild nautiluses have been caught as deep as 500 metres, but we think that such dives are very brief.
My involvement in nautilus research began in the 1970s. As a palaeontologist, I was interested in what the living nautiluses could tell us about their extinct relatives, including the ammonites. So I headed to their territory, starting in New Caledonia, then Fiji, Vanuatu, the Philippines and the Caroline Islands.
I wasn’t the only palaeontologist interested in nautiluses. Around the same time, Bruce Saunders of Bryn Mawr College in Pennsylvania set up a lengthy tag-and-release programme in Palau, and made pioneering discoveries about the nautilus’s behaviour and life history. Saunders and I eventually joined forces to study the nautilus’s evolutionary history and the relationships between the living species.
We had the great honour of being the first humans to see living representatives of many nautilus species that had previously been defined on shell characteristics alone (one species, Allonautilus perforatus, is still known only from empty shells).
The greatest surprise came from the first glimpse of what was then called the king nautilus (Nautilus scrobiculatus). It turned out to be very odd, with strange protuberances from its head, and a thick, almost hairy outer skin called a periostracum. These coverings are found on the shells of some other molluscs but were hitherto unknown in cephalopods. The king nautilus is now commonly referred to as the crusty or hairy nautilus.
The goal of our research was to understand the genetic relationships between the living species. We got some results using 1980s technology, but soon afterwards the great revolution afforded by mitochondrial gene sequencing became available. Using this technique on tissue samples gathered by Saunders and myself, Charles Wray of the American Museum of Natural History found that there were two very distinct groups of nautilus – the hairy form and all the rest.
Most of the species recognised at that time, including the relatively common emperor nautilus (Nautilus pompilius, see Map), were biologically quite similar. But the hairy nautilus stood out. In terms of its DNA, shell form and soft-part anatomy, it was separated from the rest by a wide evolutionary gulf.
In 1997 Saunders and I formally proposed a new genus, Allonautilus (the “other nautilus”) (). We were not without trepidation, for mollusc taxonomists are a conservative bunch, but we soon won the support of Steven Jay Gould, himself trained as a mollusc systematist. Other groups later produced independent evidence of large genetic differences between Allonautilus and Nautilus, and the genus has now been officially accepted, with the king (or hairy) nautilus as its type species. This was how things stood until recently.
In the past couple of years, a vigorous, new attempt to understand the evolutionary history of the living nautiluses has been undertaken. James Bonacum of the University of Illinois, Urbana-Champaign, joined forces with palaeontologists Neil Landman of the American Museum of Natural History and Royal Mapes of Ohio University in Athens to conduct the most comprehensive study yet of living nautilus genomes. Their initial findings, announced at a meeting last September, have revealed much information about the recent evolutionary history of the nautiluses.
They showed that the living nautilus lineage originated around New Guinea, perhaps as recently as two million years ago. Soon after, Allonautilus split off from the main lineage, which then began a voyage of rapid colonisation and evolutionary change.
Bonacum’s team showed that one lineage of Nautilus voyaged from New Guinea to the more easterly archipelagos of New Caledonia, Fiji and Samoa. Another made its way to Australia, Palau, the Philippines and the South China Sea.
This seafaring came as a surprise, as nautiluses seem uniquely unsuited to long-distance dispersal. Because of their depth limitations, and also because they rarely swim out of sight of the bottom and never in open water over depths that would cause them to implode, they do not easily travel to distant places. Perhaps falling sea levels during Pleistocene glaciation events allowed them to travel far afield. Or maybe rare “sweepstake” events – the term biologists use to describe very rare transportations of species to a new habitat – did the trick.
“The seafaring came as a surprise, as nautiluses seem unsuitable for long-distance travel”
However the dispersal happened, results continue to come in that change the view of nautiluses as living fossils. A few years ago, Andy Dunstan, head of research at Undersea Explorer, a commercial dive boat company based in Port Douglas, Queensland, became interested in nautiluses and tried dropping traps around Osprey Reef. He was soon catching nautiluses by the dozen, but they were quite different from the Nautilus pompilius and Nautilus stenomphalus that live on the parts of the Great Barrier Reef nearest to Osprey Reef. By X-raying the shells to count the chambers, Dunstan confirmed that the Osprey nautilus was Nautilus pompilius, but that it was much smaller than members of that species found on the Great Barrier Reef.
Dunstan’s nautiluses turned out to be dwarfs, which makes evolutionary sense, since the Osprey population is isolated on a relatively small “island” habitat surrounded by unnavigable deep water. Many species stranded on island habitats evolve dwarfism, driven by selection for more efficient use of scarce resources. The classic example is the mammoths of Wrangel Island in Siberia, which, once cut off from the mainland population, became pony sized.
Dunstan began trapping nautiluses elsewhere around the Great Barrier Reef, and was soon joined by geneticist Billy Sinclair of Central Queensland University in Rockhampton. Their DNA work adds new depth to the emerging picture of numerous episodes of dispersal, isolation and evolutionary change ().
The idea of nautiluses as living fossils now has to be rejected. Bonacum recently told me that he believes the Osprey Reef nautilus is a separate species. In fact, he favours scrapping the species Nautilus pompilius altogether since it is meaningless – it encompasses tens of distinct species. What we are witnessing is not the final flickering of an ancient group, but a vigorous radiation of new species.
It is a final aspect of the Osprey Reef work that brought me back to these animals. In the early 1980s, I used acoustic transmitters to track nautiluses in Palau, New Guinea and New Caledonia. The work showed that nautiluses follow quite a regular behaviour pattern – they spend their days at depths of 300 to 400 metres and then, at sunset, swim vigorously towards the surface to feed. In New Caledonia, they come all the way to the top, the only place in the world where divers routinely see them in the wild.
Dunstan – now at James Cook University in Queensland – proposed to do the same kind of work at Osprey and invited me to join him. We first tried it in August 2007, but got no results. The saddles that attached the transmitters to the shells were faulty, and the nautiluses bucked them off. In December we tried again, and this time succeeded. The results are still coming in and the details are under wraps, but it looks like Dunstan has discovered a kind of nautilus behaviour unlike any observed elsewhere. This is yet more evidence that the Osprey Reef nautilus is a separate species.
This new era of nautilus research is just beginning. There are still more questions than answers, most importantly about the fine details of the recent evolutionary radiations and colonisations. New trips are being planned, some to study the elusive Allonautilus in its native habitat, including Allonautilus perforatus, which may turn out to be a subspecies of scrobiculatus.
Unfortunately, time is not on our side. The great survivors are facing their greatest challenge – humans. Caught for their shells, which are sold as souvenirs or turned into buttons, nautilus numbers are declining. One population in the Philippines has already been wiped out, and fleets of nautilus boats are now moving farther up the South China Sea. The nautilus has survived all that Earth could throw at it. It’s up to us to make sure it doesn’t get driven to extinction by the most voracious predator of all.
Evolution – Learn more about the struggle to survive in our comprehensive special report.
