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Life underground, down under
06 August 2005
From New Scientist Print Edition.
Stephanie Pain
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Land of plenty

There you are, driving across the hot, dry centre of Western Australia. It's desert really. Not sandy like the Sahara, but red and rocky with a sparse covering of mulga scrub. The dirt road throws up red clouds of dust, and other than the occasional termite mound or stunted tree there's nothing to break the monotony of the landscape.

Then you see him. Out in the waterless desert, there's this guy sitting on a little stool - fishing. Fishing? You slow down, not too much - you get some strange people out here - but enough to see he is reeling out a line. If you stopped to ask, you would discover that the line doesn't run into the dust but passes through a small hole in the ground and down into a subterranean world as unexpected as the sight of a man fishing in the desert.

The man isn't crazy, he's a stygobiologist and he's fishing for stygobites. Named after the river Styx, which in ancient Greek myth carries the souls of the dead to Hades, stygobites are the creatures that inhabit the watery regions of the underworld. Just a few years ago Australia wasn't even on the map as far as stygobiologists were concerned. Now it's the world's hottest spot for stygofauna. The reason? Beneath the arid surface of Western Australia are hundreds of limestone deposits honeycombed with small holes and filled with water. Each of these deposits is teeming with life. And in each case it's different.

These latest additions to Australia's fauna offer tantalising glimpses of long-lost worlds, drifting continents and the processes of evolution. But biologists aren't the only ones interested in the steady stream of weird and wonderful creatures emerging from under the desert. Stygobites are a hot topic in the boardrooms of Australia's mining companies too. Under Western Australian law, it is illegal to drive a species to extinction, and mining could all too easily wipe out entire stygofaunas. In 2001 discovery of small shrimp-like creatures at a site operated by mining giant BHP Billiton brought work to a halt for 10 months. So in an unlikely alliance, the industry has joined forces with the stygobiologists to find out more about life underground.

In the past, the richest hunting grounds for stygobites were Europe and North America, continents with extensive regions of karst - a landscape of limestone caves and tunnels, and underground streams, rivers and lakes. Early explorers of these watery caverns returned with specimens of pale, blind fish, eyeless salamanders and a host of invertebrates - translucent crayfish and other crustaceans, worms, snails and occasionally aquatic insects. These animals had lost features useful on the surface, including eyes, pigmentation and wings, but gained others that helped them cope with cave life, such as flattened, flexible bodies for squeezing through tight spaces, and well-developed senses for finding food in the dark. According to conventional wisdom, most stygobites went underground to escape the rigours of the ice ages of the Pleistocene epoch, which began around 1.8 million years ago.

Over the past few decades, stygobites have been discovered in ever smaller and more inaccessible places - almost everywhere there is a water-filled space in a rock, in fact. But no one expected to find them in the Australian desert, says Bill Humphreys, an invertebrate specialist at the Western Australian Museum in Perth. "Australia was considered the least likely place on Earth to find stygofauna," he says. "It's too arid, there isn't much karst and it wasn't covered with ice during the Pleistocene."

Humphreys suspected otherwise. He had an idea that in Australia, the drying out of the continent during the earlier Miocene epoch might have triggered an exodus from the surface in the same way that expanding ice sheets did in Europe and North America. The drying trend began around 30 million years ago, as the continent drifted north from Antarctica. By the late Miocene, around 12 million years ago, permanent dryness set in across the northern part of the continent and slowly spread south. Humphreys also had a hunch that if there were stygobites beneath the desert, some of them might be "ghosts", rare survivors of groups that have long since vanished from the world above. And he had a good idea where to look for them.

Australia's western plateau is dotted with limestone deposits, laid down along the routes of ancient dried-up rivers during a dry phase between 37 and 30 million years ago. These "calcretes" formed in places, usually upstream of salt lakes, where groundwater flowing beneath the old riverbeds came close enough to the surface to evaporate. After they formed, the climate became wetter and rivers returned to the old channels, dissolving the limestone until it resembled small-scale karst, riddled with tiny voids and tunnels rather than caverns and potholes. When the Miocene drying emptied the river valleys once more, the calcretes remained - and remain - filled with water. Humphreys figured that if there were stygobites under the desert, these were the places to find them.

There are more than 200 major calcretes in Western Australia and many more smaller ones, with concentrations in the Yilgarn and Pilbara regions (see Map). The deposits are about 10 to 15 metres thick, but many cover vast areas, and because they trap and store groundwater they form sizeable aquifers. Most lie close to the surface, just below the water table, but you can't get inside a calcrete as you might a cave. The only way in is via wells and boreholes dug by cattlemen and miners (see "Into the underworld"). In 1998, Humphreys dropped a line down some of these and immediately found species no one had come across before. The arid-country calcretes were definitely worth some serious investigation.

“Anyone driving past must think we're crazy. Fortunately there aren't many people out here”The past five years have seen a growing band of stygobiologists heading for the outback with fishing rods and plankton nets. "Anyone driving past must think we're crazy," says Steve Cooper of the South Australian Museum in Adelaide. "Fortunately there aren't many people out here." To date, Humphreys and a team of biologists from the University of Western Australia in Perth and the South Australian Museum have sampled more than 80 calcretes. Almost everything they have brought up - more than 200 species so far - has been new to science. More exciting still, every calcrete has its own distinct fauna. "Each calcrete is a sort of underground island of water cut off from the others, which means each group of animals has evolved in isolation," says Cooper.

"On the surface the landscape is harsh and dry. You wouldn't think it was a hotspot for aquatic life," says Terrie Finston, a molecular biologist at the University of Western Australia. "But underground the diversity is incredible." For some groups of animals, subterranean species outnumber surface-dwellers. The shrimp-like amphipods are especially diverse, with perhaps 10 times as many species below ground as on the surface. The Pilbara calcretes are rich in another group of crustaceans, the ostracods, which are as diverse as those in Russia's Lake Baikal, the world's deepest lake and one of the largest. Other crustaceans, such as copepods and isopods, are plentiful too. Because of the confined space, there are no fish or amphibians but there are a few types of worm and snail and, most spectacularly, in the Yilgarn calcretes there are getting on for 100 species of diving beetles. "That's 10 times as many as anywhere else in the world," says Chris Watts, a beetle specialist at the South Australian Museum.

Mysterious ways

So far there is only a sketchy picture of how the animals live. For the moment, the stygobiologists are asking the most basic questions: What do they eat? How do they reproduce? Where does a beetle larva go to pupate - something terrestrial species do out of water. Without direct access to the calcretes, it is hard to know. What is certain is that space is tight. "We often wonder where the animals actually live," says Humphreys. As for food, they most probably graze on films of bacteria that live off dissolved organic matter carried in by groundwater. Others eat detritus, but some stygobites are almost certainly carnivorous. "There's one amphipod we call velociraptor, because its huge front appendages make it look predatory," says Finston.

The diving beetles also seem to have kept their carnivorous habits below ground, if their huge jaws are any guide. Cooper has been observing live beetles in his lab, but so far they haven't given away much. "They seem to tuck into mushed amphipod, but we don't know if they hunt them. They could be scavengers." There's little doubt when it comes to their larvae, though: their jaws are truly terrifying.

Cooper has established that subterranean beetles lead slower lives than those in the outside world. "Diving beetles are extremely active and zip to the surface all the time to breathe. Our beetles seem to crawl slowly about on the bottom. I rarely see them come to the surface for air," he says.

There is a question mark, too, over how animals thought to belong in fresh water survive in many of the calcretes, where the water can be fresh, brackish or as salty as the sea - and can fluctuate wildly. Rain is sporadic but torrential. If the dry period is prolonged, the water becomes saltier; when the rains come there is a sudden influx of fresh water. "It's a simple ecosystem but it can be quite dynamic chemically," says Remko Leys of the South Australian Museum. "These animals have had to adapt physiologically as well as anatomically to life in the calcretes."

The stygobiologists are making headway with some bigger questions about when and why these animals left the outside world and headed underground. There is circumstantial evidence to support Humphreys' conviction that the spread of aridity that began in the Miocene was the main driving force: where stygobites have surface relatives in Australia, they are confined to the wetter regions of the continent, and where it is wet there are no subterranean species. If he is right, then as the rivers of the western plateau began to dry up, their faunas would have sought refuge in the waterlogged sands and gravels of the riverbed, where they adapted to life in the spaces between stones or sand grains. And when even that water disappeared, they went deeper, into the underlying groundwater, and some found their way into calcretes. Isolated in separate calcretes, they began to diverge, eventually evolving into the array of species living there today. There are some surface beetles that seem to be going down this route even now. They live in sandy gravels alongside streams that dry out in summer, and show early signs of adapting to life below ground. "They still have wings but their eyes are obviously reduced," says Watts. "We guess this is what happened."

Looks can be deceptive

If it is, then you would expect to find patterns in the way related species are distributed, reflecting when and where their ancestors went underground before evolving into new species, first in the drying river bed and then in the confines of the calcretes. You would expect, for instance, that those in deposits along the same river catchment should be more closely related to each other than to those in calcretes along different river systems. Finding hard evidence to support the theory depends on knowing exactly where the different species lie on their family tree. But living underground has led to the evolution of characteristics that can confuse even the most experienced taxonomist. These animals have lost many familiar features, such as eyes and hard parts that might hinder movement in tight spaces, and most have acquired a very similar body shape. Many species that are only distantly related appear practically identical. "Their adaptations to subterranean life can throw you off the scent in a big way," says Watts.

To frustrate their efforts further, some closely related species look utterly different. The beetles are a particular challenge. "Above ground, diving beetles are similar, with bodies streamlined for fast swimming and rapid diving," says Watts. "But underground, they are released from whatever pressure leads to that uniformity and are all sorts of bizarre shapes and sizes." Particularly baffling are the weird genitalia that some possess. "Above ground their penises are very uniform. Below, they are bizarre. We have no explanation," says Watts.

Fortunately, taxonomy no longer depends entirely on observation - counting appendages or getting to grips with the finer details of invertebrate genitalia. Molecular biologists can draw up accurate family trees showing how species are related by comparing certain proteins or key stretches of DNA. Finston has used these techniques to map patterns of genetic variation in a group of amphipods living in the Pilbara calcretes. Her results show that those living in different river systems are indeed more distantly related than those living within the same one. She can also put a rough date on when they went underground. Because genetic mutations occur at a reasonably regular rate, by comparing DNA from amphipods in different calcretes, she can estimate when their common ancestor abandoned life on the surface. "Individuals in different river systems last shared a common ancestor in the late Miocene, some 10 to 13 million years ago," says Finston. This matches the time when aridity had settled in for good in the Pilbara region. "And we see a similar pattern with isopods," she says.

In the Yilgarn, the diving beetles tell a similar story of the aridity that crept slowly southwards across the land. But unlike the amphipods' ancestors, the beetles' forebears could fly, which led to a different pattern of colonisation. Each of the calcretes where beetles have been found contains a unique assemblage of species - most often three, but sometimes one, two or four. In most cases, the species in the same calcrete are not close relatives. This suggests that there were multiple invasions by ancestral species that had wide ranges extending across many river catchments, and that when the water disappeared, they went underground wherever they happened to be.

Ghosts from Gondwana

In 15 calcretes, however, Watts and his colleagues have found pairs of "sister" species. "We think they evolved in the calcretes - probably at the time of the transition to underground life," says Leys. Why a single population should have evolved into two species is puzzling. There is evidence to suggest that this is an intriguing, rare example of "sympatric" evolution, where speciation occurs even though members of the original population have not become physically isolated. This excites Leys for another reason. The DNA of sister species shows when their common ancestor entered the calcretes. This time the date is around 5 million years ago - which is when many river systems became permanently dry in this region.

“Above ground the beetles' penises are very uniform. Below, they are bizarre”But this is clearly only part of the story, because the calcretes also contain some far more ancient groups of animals. The Yilgarn and Pilbara regions both lie on one of the world's truly ancient continental land masses, a part of the country that has stood above sea level for more than a billion years. Humphreys was originally drawn to the region in the hope of finding stygobites that might be descendants of creatures that swam in rivers and lakes when Australia was part of the southern supercontinent Gondwana, 200 million years ago or more. He has not been disappointed.

In the Pilbara, for instance, there are two species belonging to a primitive group of crustaceans called the Spelaeogriphacea. There are only two other known species: one lives in a cave on South Africa's Table Mountain and the other in caves in the Matto Grosso of western Brazil. Their strange distribution reflects the break-up and movement of continents over many geological ages. The ancestral spelaeogriphids were marine and widely distributed in the ancient Tethys sea. Some invaded fresh water in Gondwana and then they all went extinct - except for a few species that had found safety in the underworld before disaster overtook the rest. When Gondwana broke up and the southern continents drifted apart, these subterranean survivors were scattered around the globe.

Other survivors from the distant past are primitive groundwater crustaceans called bathynellids. They arose in Pangaea and can still be found in groundwater around the world. But the modern forms are typically tiny - around a third of a millimetre long - and live between sand grains in freshwater aquifers. "We've got giant ones around eight millimetres long living in highly saline groundwater," says Humphreys. "These live free and swim like seals. And they are the spitting image of the hypothetical ancestral bathynellid." This suggests that this bathynellid is a "ghost", a species stuck in a time warp in its subterranean hideout while those in the world outside went down another evolutionary path.

These ancient creatures must have colonised the underworld long before the calcretes had formed, says Humphreys. "We have no idea when or why they went. But whatever the reason, they must have gone underground somewhere else and moved in as the calcretes became available."

Of all the questions still unanswered, perhaps the most important is whether the stygobites can hang on in their desert refuges. Much of the region is pastoral land, and cattle need water, much of which is pumped up from the calcrete aquifers. But this is also the most mineral-rich region of Australia, with massive deposits of iron ore, as well as gold, nickel and uranium. "There are mines dotted all over the place and most of the towns are based on mining," says Cooper. Miners, like cattle, need water. But the gravest risk comes from "dewatering", an operation to lower the water table at opencast sites to make it easier to excavate ore. "If the water table drops below the calcrete there is likely to be immediate extinction of everything in it," says Cooper.

Until very recently, no one was aware these stygobites even existed. Now, thanks to a law introduced to conserve more familiar animals and plants, the industry must show that its operations won't harm them. Ironically, by funding research to find out where the stygobites are and whether it might be possible to use "their" water without destroying them, big business is helping to solve some intriguing evolutionary puzzles. "What we have here is unique in the world," says Cooper. "And we've only just begun to explore it."

From issue 2511 of New Scientist magazine, 06 August 2005, page 28

Into the underworld

Cave biologists can usually walk, crawl or wriggle to work, but Australia's new breed of stygobiologists can only find their quarry with the aid of a good geological map, a fishing rod and a handy hole. Fortunately, the dry parts of Western Australia are dotted with wells and boreholes that penetrate the water-filled calcretes. "In pastoral country there's a well built every 10 kilometres, which is about as far as cattle can walk," says Bill Humphreys of the Western Australian Museum. "But more and more we are finding old mineral exploration bores that were drilled then sealed up again. Some of these are in regular grids, which is handy for sampling."

"Some calcretes have been exposed by mining, so we've seen what they look like inside," says Chris Watts from the South Australian Museum. But when stygobiologists cast their lines into these labyrinthine habitats, they are as much in the dark as the animals they are hunting. Recently, the team tried some down-hole photography, lowering a mini video camera into the void. The view is limited, but they have caught glimpses of some of the larger stygobites in their natural habitat.

Without a better way of viewing what goes on, some aspects of subterranean life remain a mystery. What does seem certain, though, is that there are many more stygobites down there. "Some of the wells are a century old, yet no one had ever seen a diving beetle in one before," says Watts. "It's only once you start looking for things that you find them."

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