Australasian Science: Australia's authority on science since 1938

The First Breath

Image of lungfish ribs

The cranial ribs in the Australian lungfish Neoceratodus forsteri are needed to anchor the pectoral girdle, allowing the fish to raise its head to gulp air. Image adapted from Johanson et al. 2005.

By Alice Clement

A new fossil find shows that a global decline in oxygen millions of years ago drove the evolution of air-breathing in lungfishes.

Most people enjoy a dip in the ocean at their local beach or favourite holiday spot, but if you lived during the Devonian you might think twice before taking the plunge.

The Devonian Period, 416–359 million years ago, is known as the Age of Fishes. Life in the seas was very different to what we know today. The waters teemed with a plethora of beasts, including huge armoured placoderm fishes and early sharks and bony fishes. Nautiloids floated by while trilobites (ancient arthropods) scuttled around beneath them.

At this time, some fishes were invading near-shore and freshwater habitats, perhaps to escape the dangerous Devonian seas. Others, such as the early tetrapods, were beginning to venture onto dry land.

Migrating out of the water and onto solid earth was no easy feat. These animals would have faced new challenges relating to locomotion, regulation of water content and respiration.

The tetrapods were not the only ones using lungs instead of gills. Lungfish, our closest surviving piscine relatives, independently developed the ability to breathe air during the Devonian Period. Lungfish surviving today inhabit freshwater territories, and lungfish fossils thought to have been air-breathers have all originated from swamps, lakes and river deposits (i.e. freshwater environments).

Warm, stagnant, tropical swamps were long thought to be the setting for the evolution of air-breathing in both tetrapods and lungfish, and the fact that freshwater environments often have lower oxygen levels than marine waters lent support to this theory. However, a new fossil discovery from Australia is now challenging this accepted hypothesis.

The Gogo Formation in the north of Western Australia represents one of the best Devonian fossil sites in the world. These gigantic ancient reefs were the homes of many creatures, and were built largely by algae and bacteria – unlike the coral reefs of today.

Gogo once abounded with prehistoric fish, but it is the nature of the fossil preservation that makes Gogo so special. Here, fossils are preserved in rounded limestone concretions that formed rapidly around the fish skeleton, preserving it in perfect 3D (AS, July 2008, pp.16–18).

I visited Gogo last year as part of a joint Museum Victoria/Australian National University expedition led by Dr John Long (AS, October 2009, p.41), who has been collecting at the site since 1986. Also on the expedition was Dr Anne Warren of La Trobe University, who discovered a remarkable specimen that would turn out to be a new species of lungfish never seen before.

The new lungfish, a species of Rhinodipterus, was even more exciting than John and I first thought. Careful preparation using weak acetic acid to dissolve away the limestone revealed Gogo’s first air-breathing lungfish. In fact, this was the first unequivocal marine air-breathing lungfish ever!

A number of key features of the skeleton, many of which can be seen in living lungfish, indicate that Rhinodipterus could gulp air. These include a long mouth cavity that could hold a large air bubble, and highly moveable pectoral and gill elements to create a vacuum inside the fish’s mouth.

Paired structures called cranial ribs are important in the air-breathing behaviour of living lungfish are also found in Rhinodipterus. The function of cranial ribs was first demonstrated in 1968 when two British scientists, Dr George Foxon and Dr Ian Bishop of Guy’s Medical Hospital, London, analysed how the African lungfish respired by filming the action with an X-ray video camera. They discovered that the cranial ribs were needed to anchor the pectoral girdle, allowing the fish to raise its head so that it could take a gulp of air.

Our discovery raised many questions. What was the driving force for air-breathing? Did it evolve in marine or freshwater? And why would a marine fish need to breathe air?

As this specimen was undoubtedly marine, we investigated environmental factors other than habitat for the answers. What we found was that during the Devonian there was a plunge in global oxygen levels, which fell as low as 12% (compared with current levels of 21%).

Evidence for this global oxygen decline comes from the relative abundance of charcoal at the time. Charcoal can be used as a proxy for fire in the fossil record. Fire can only occur when oxygen levels are within a 13–35% concentration in the atmosphere. Thus a paucity of charcoal in Middle to Late Devonian deposits indicate global atmospheric oxygen depletion during this time.

Further evidence comes from changes in the geochemical cycles of carbon and sulfur. Weathering of carbon and sulfur consumes oxygen, and thus will lower its concentration in the atmosphere. This weathering occurs when there is a high instance of tectonic uplift, erosion and exposure of coastal lands by sea level changes. The long-term geochemical cycles of these elements point to low oxygen levels during the Devonian.

A worldwide fall in oxygen would have affected both marine and freshwater lungfish alike, with the effects of oxygen depletion driving accessory air intake in other fishes as well. Another Gogo fish, Gogonasus, a close ancestor of the land animals, had large holes on the top of its skull called spiracular notches that may have supplemented oxygen intake to the gills and lungs.

This evidence suggests that the fish at Gogo were oxygen-stressed, and they responded by evolving adaptations to cope with this pressure.

As life became more diverse and complex in the Devonian, it is likely that fish needed more energy to survive in an arms race against competitors, predators and changing environmental conditions. More oxygen means more get-up-and-go, and more likelihood of out-swimming your predator or catching your dinner.

The Australian lungfish Neoceratodus lives today in the rivers of southern Queensland. "It doesn't need to breathe air, but does so to supplement its oxygen intake when hunting or at its most active. This behaviour may have also helped its prehistoric relatives to survive, especially in times of depleted oxygen.

We have concluded that a huge plunge in global oxygen, possibly combined with higher metabolic costs, drove the evolution of air-breathing in lungfishes during the Devonian Period.

This discovery is important as it changes our ideas about the selective pressure behind air-breathing. The driving forces shaped not only the evolution of the lungfishes, but the line of fishes that led ultimately to us. Thus these events are as much a part of our own history as they are of the lungfishes.

Alice Clement is a PhD student at the Research School of Earth Sciences of the Australian National University and Museum Victoria, where she is studying lungfish evolution and anatomy.