At the bottom of the Arctic Ocean, in cold dark waters miles away from anywhere, lie five active volcanoes.
But these are not your typical volcanoes, belching out hot molten lava. They are mud volcanoes, and as the name suggests they are spewing out warm mud – as well as methane gas.
It sounds pretty inhospitable, and to humans it would be, but these strange volcanoes are home to billions of small worms. These creatures survive without light. But how they do it is only just starting to be revealed.
The story begins in 2009. Scientists from the ArcticNet project were on a research ship, using sonar to map part of the Beaufort Sea, which lies north of Canada and close to Alaska. They discovered large circular structures between 250 and 750m below the surface.
The team had only a short window before the sea ice became too thick
Changes in the sound waves reaching the ship suggested that large volumes of gas were bubbling up from the sea floor: a sign of volcanic activity. The most likely culprits were mud volcanoes.
These are formed when a vent in the Earth's surface releases gases. Mud flows from the seafloor and forms a cone-shaped mound around the vent. Compared to normal volcanoes, mud volcanoes are much cooler.
In 2013 a team of scientists from around the world decided to take a closer look. They set sail aboard the Canadian icebreaker CCGS Sir Wilfrid Laurier (SWL).
The expedition was one of the first of its kind to take place in the Arctic Ocean. Working in October, the team had only a short window before the sea ice became too thick – making the area above the mud volcanoes inaccessible and potentially trapping them there.
The volcanoes are so large that you can only see a small part of them at any one time
The first thing the team needed was a detailed map of the area. To get this, they programmed an autonomous underwater vehicle (AUV) shaped like a torpedo to fly down to 50m above the seabed. Once there, the AUV moved back and forth over the area, much like a person mowing a lawn.
The resulting map revealed five giant mud volcanoes. They were 600 to 1,100m across, and up to 30m tall.
Next the scientists wanted to see them close-up. For this, they used a remotely-operated vehicle (ROV) that beamed back a live high-definition video of the sea floor.
It showed that most of the mud volcanoes had remarkably flat tops surrounded by a circular ridge.
"The volcanoes are so large that you can only see a small part of them at any one time," says Charlie Paull of the Monterey Bay Aquarium Research Institute in Moss Landing, California, US. "They erupt frequently and release gas and mud, which bubbles out onto the seafloor. The mud has a viscous texture like the top of a very thick stew."
The world's mud volcanoes are estimated to release 27 million tonnes of methane every year
The eruptions contain many different chemicals. First on the list is methane, otherwise known as natural gas.
"The gas coming out of the volcanoes is biogenic methane, which means that it is produced by the decomposition of organic matter and bacteria, and not from oil deposits trapped underground," says Paull.
A lot of Earth's methane is trapped below the seabed as "gas hydrate", an ice-like crystal of methane and water. Hydrates form when the intense pressures at depths of over 500m freeze the methane and water. When mud volcanoes erupt near gas hydrates, the methane in the hydrates can escape, along with methane from deep underground.
The world's mud volcanoes are estimated to release 27 million tonnes of methane every year, about 5% of annual global emissions.
The Beaufort Sea volcanoes also spew out water rich in dissolved compounds, such as sodium bicarbonate. The water seems to be a mixture of seawater, water from snow and rain, and water from deeply-buried clay.
The ROV's cameras revealed vast thickets of worms
"When clay minerals get buried they are exposed to increasing pressure and temperature," says Paull. "The pressure causes the clay structure to change, which results in a release of water from the clay."
And then, of course, there's the mud, which spills out onto the cold floor of the Arctic Ocean.
It is nowhere near as hot as a molten lava eruption, and quickly gets cooled by seawater. Still, the frequent eruptions warm the seas, and water temperatures as high as 9.1 °C were recorded around the flat tops of the volcanoes.
It seems the volcanic activity acts as a beacon, attracting life to the area. Along the slopes of the mud volcanoes and their flat tops, there are vast communities of tubeworms.
The ROV's cameras revealed vast thickets of worms. A small mechanical arm attached to the ROV grabbed some of these worms and carried them back to the surface.
The Beaufort Sea tubeworms are only 7-8cm long. However, they are distantly related to giant tube-dwelling annelid worms that are found near deep-sea hydrothermal vents. Such worms can be 2m long.
I think it's likely that bacteria living inside the tubeworms are doing all the work
Both groups of worms survive without light, under intense pressures and in water that is often laced with acid and toxic gases. They can cope with a wide range of temperatures. Often one end of a tubeworm can experience near-freezing temperatures, while the other end is exposed to hot fluids flowing out of the seafloor.
They have no eyes, no stomach and no anus. Instead, they somehow feed on the gases pumped out of the volcanoes.
The scientists aren't sure whether it's the methane gas itself that the worms feed on, or hydrogen sulfide, which is made when the nearby microbes oxidise methane.
"The tubeworms are using either methane or hydrogen sulfide as an energy source," says Paull.
The process is called chemosynthesis. The worms perform a chemical reaction, either on methane or hydrogen sulphide, and this releases electrons – which supply energy.
The tube worms seem to prefer some areas of the volcanoes over others
"The tubeworms probably aren't performing the reaction themselves," says Paull. "I think it's likely that bacteria living inside the tubeworms are doing all the work. The tubeworms bring in methane and oxygen, the two things that bacteria need, and the bacteria get to work synthesizing new organic matter."
If that is true, the worms are "farming" the bacteria within their guts. They provide a stable, chemical-rich environment for the chemosynthetic bacteria, which in turn serve as food for the worms.
Hydrogen sulfide has the advantage that the worms can turn it into sulfur, which they can store much like our bodies store fat. They cannot store methane, and have to use it there and then.
Interestingly, the tube worms seem to prefer some areas of the volcanoes over others.
The worms were primarily found on the flat tops of the mud volcanoes, not on the slopes. The size of these colonies ranged from 10cm across, with only a few dozen worms, to extensive thickets of worms filling most of the ROV camera's field of view.
In 2000, researchers found tubeworms that took 170-250 years to grow 2m long
The thickets, which Paull describes as "as dense as grass in a hayfield", contained millions of worms. They were clustered around old mud flows. This makes sense, because the tubeworms need a steady supply of either methane or sulfide to survive, and the mud flows would provide that
However, there were no worms around the newer mud flows, even though they are richest in methane. One of the volcanoes, which was both the youngest and the most active, was almost devoid of worms.
"This volcano is different because it is the youngest," says Paull. It may be that this mud volcano is so active, and the mud flows on it so young, that the worms haven't yet been able to colonise it.
The tubeworms may simply be growing very slowly.
Some tubeworms are remarkably long-lived. In 2000, researchers found tubeworms that took 170-250 years to grow 2m long. They lived in cold seeps, another type of chemosynthetic environment, around the Gulf of Mexico.
We do not yet know how quickly the Beaufort mud volcano worms grow. But having such a slow growth rate would make them slow to colonise the mud flows, explaining why the new mud flows are uninhabited.
The whole setup is eerily similar to another mud volcano, on the other side of the world
The speed at which the mud volcanoes erupt and change may also explain why they are, apart from the worms, more or less uninhabited.
"We didn't see the common hallmarks associated with other methane and hydrogen sulfide environments, such as various types of clams, mussels and bigger tubeworm species," says Paull. "I personally think that that's because the top of the volcanoes are churning over too fast for worms and other animals to accumulate there."
You may think it would be a disadvantage for a slow-growing tubeworm to live in a dynamic environment such as a mud volcano, as it might not have time to breed before being buried by boiling mud. However, it is not clear that the eruptions directly harm the worms once they are in place.
The whole setup is eerily similar to another mud volcano, on the other side of the world.
A genetic analysis of the Beaufort tubeworms shows that they are closely related to siboglinid tubeworms living on the Håkon Mosby mud volcano, in the Norwegian Arctic.
Mud volcanoes like Håkon Mosby and the Beaufort Sea volcanoes remain mysterious
The Håkon Mosby volcano was discovered in 1989 by researchers at the University of Bergen. It lies 1250m beneath the sea, much deeper than the volcanoes in the Beaufort Sea. It is also much flatter, only rising 10m above the ocean floor. It covers an area of about 2 sq km and belches out mud, water and methane from its centre.
Every year, Håkon Mosby emits several hundred tons of methane. It is thought to have been active for at least 40 years. The methane is a greenhouse gas, but most of it never makes it to the atmosphere, as microbes and tubeworms break it down.
In fact, mud volcanoes like this may be remarkably common.
A study published in 2000 estimated that there are between 1000 and 100,000 mud volcanoes in the deep sea – plus all the ones on land.
We are only just scratching the surface of these underwater volcanoes
Yet despite this, mud volcanoes like Håkon Mosby and the Beaufort Sea volcanoes remain mysterious. We do not even understand why they are so active.
Normal volcanic eruptions can be triggered by earthquakes and shifting tectonic plates. But earthquakes are rare in the Arctic. Scientists took seismic measurements of Håkon Mosby from 2008 to 2010, and found no clear evidence that tremors triggered eruptions.
Researchers believe that a series of chambers beneath the volcano, possibly reaching as deep as 1000m beneath the seafloor, are feeding methane gas and mud to the mud volcano. Similar chambers could exist below the Beaufort Sea volcanoes.
We are only just scratching the surface of these underwater volcanoes. But now is the time to find out.
The Arctic is warming due to man-made climate change, and many countries and companies are interested in sending shipping through, or exploiting its vast reserves of oil and gas. If we are to protect its unique marine life, including the tubeworms of the Beaufort Sea, we will first need to understand them.