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YOU ARE standing in a primeval forest during the Carboniferous period, 300 million years ago. Dragonflies with wings almost a metre across weave in and out of trees that tower 50 metres above you. On the ground, huge amphibians 5 metres long amble past – but watch your step, there are also metre-long millipedes and scorpions to avoid.

And there’s something about the air: breathing it is beginning to make you feel a little light-headed. That’s because it contains nearly 50 per cent more oxygen than the stuff we breathe today. And that, researchers now believe, is why these giant plants and animals evolved – and what, in the end, may have destroyed them.

It is now widely accepted that oxygen levels fluctuated widely over geological time and that oxygen-rich air might explain the evolution of these massive animals, and possibly even flight itself. Some speculate that high oxygen levels could have triggered global firestorms, and might even have contributed to the demise of the dinosaurs.

These are important questions, because the response of life to an oxygen-rich atmosphere might explain more than what happened in the past: it could help inform our future too, warning us of the potentially devastating consequences of global warming, for example. And if oxygen levels really did rise so high in the past, why did that swell some creatures to massive proportions, rather than accelerate their ageing and send them to an early death? Perhaps these primordial giants can give us some tips for a longer and healthier life?

Experts squabble about how all this extra oxygen got into the air. Virtually all the stuff around today is a by-product of photosynthesis. Using energy from sunlight, plants and green algae convert water and carbon dioxide into carbohydrates and other organic carbon compounds, releasing oxygen in the process. Respiration does pretty much the reverse, converting oxygen and carbon compounds into CO₂ and water. These two processes work in almost perfect equilibrium, with the result that even above the Amazon rainforest there is next to no extra oxygen in the air: whatever the lush greenery creates is consumed by the exuberant army of monkeys, birds, fungi and bacteria. It’s a similar story in the oceans.

The only way oxygen can build up in the air is if some of the organic carbon is buried beyond the reach of air-breathing creatures. This means that any change in the composition of the air is dictated more by geology than biology. So if we want to know how much oxygen there was in the air 300 million years ago, we need to know how much carbon was buried underground.

Unfortunately this is no simple task. Most carbon is buried as microscopic grains trapped in sedimentary rocks such as shale and limestone. In the intervening years, much of this rock has been worn away by erosion, so where do you start?

The difficulties have not deterred Robert Berner of Yale University. Fifteen years ago Berner, with Gary Landis of the US Geological Survey in Denver, Colorado, kicked off the oxygen debate with a report in Science that tiny bubbles of seemingly ancient air trapped in chunks of amber contained half as much oxygen again as today’s atmosphere. Subsequent studies showed that amber may not be the impermeable time capsule that Berner and Landis had hoped. But keen to confirm the results, Berner decided to tackle the problem using the curious preference of living things for “lightweight” carbon.

Carbon atoms come in two stable isotopes with slightly different masses. Photosynthetic organisms slightly prefer the lighter form, carbon-12, to its heavier sister, carbon-13. As a result, organic matter becomes enriched in carbon-12, and when it dies and is buried, a slight excess of carbon-13 is left behind in the environment. This finds its way into the oceans, from where it is eventually deposited as sedimentary rock such as limestone.

Berner realised that he could trace this carbon-13 signature in limestones laid down on the seabed of ancient oceans. Increased levels of carbon-13 would point to a corresponding increase in burial of organic matter, and that would give a measure of the levels of oxygen in the air at that time. His conclusions were striking: it seemed that oxygen levels climbed as high as 35 per cent during the Carboniferous period, fell, then settled at about 25 per cent during the Cretaceous, 100 million years ago. Today the level is just under 21 per cent.

But elegant as his technique might be, it is also indirect and his conclusions are disputed by other scientists. They claim that Berner has overlooked one important factor: the Earth’s biosphere, they argue, would have acted to reduce elevated oxygen levels and would have constrained any increase in levels to about 28 per cent at the most.

The crux of the matter, they say, is fire. In an oxygen-rich atmosphere, fires would burn unusually fiercely, and would quickly consume much of the excess. But Berner says this claim is flawed (see “All well and good on paper”). And besides, he points to a more fundamental problem: rather than simply vaporising trees and other plants, fires produce vast amounts of smouldering charcoal. The diabolical catch is that a fire may be fast, but it is less efficient than respiration at converting organic matter back into CO₂. Charcoal, and the organic carbon compounds it contains, resists further breakdown, even by bacteria, and is more likely to be buried intact than any other form of organic matter. So these fires can actually increase the rate of organic burial. Perversely, says Berner, the more fire, the more oxygen.

If there really were so many fires back in the Carboniferous, there ought to be plenty of evidence in the fossil record. Plants and animals would be forced to adapt to serious new threats – not just fires, but also the increase in oxygen itself. So did they?

The signs are encouraging. Jennifer Robinson, a specialist in ancient fires at Murdoch University in Perth, Western Australia, has spent much of the past decade studying how plants in Carboniferous swamps adapted to fires. Notable among these were the giant lycopods, colossal “scale trees” with beautifully patterned bark that grew more than 50 metres tall. They seem to show numerous possible adaptations to fire, and Robinson has found unmistakable evidence of regular burning. Some coal from the period contains as much as 30 per cent fossil charcoal, implying that fires were common despite the sodden surroundings. And the physical properties of this charcoal, such as its reflectance, suggest it was formed at the searing temperatures characteristic of an oxygen-rich fire.

Even more striking are the ways animals adapted. This was an age of giants. Beneath huge lycopods, amphibians grew from newt-like proportions to reach lengths of up to 5 metres. One such beast left some of the oldest footprints in Britain, at Howick in Northumberland. Millipedes and scorpions grew to more than a metre and the Megaranea spider had a leg span of 50 centimetres.

But the most famous example is the monumental dragonfly dug up in England in 1979 below the Derbyshire mining town of Bolsover. It had a wingspan of more than half a metre, as broad as a hawk, and more than five times that of its largest modern relative. Similar giants have been found in France, Russia and America, all of them dating to the high-oxygen period.

These giant dragonflies are poorly preserved, but enough remains to see that the wing structure was simple compared with modern dragonflies. The combination of sheer size and simple structure has led some scientists to claim that they could only have got airborne if the air was denser and richer in oxygen then than it is now.

Not everyone agrees. “Why call on a special explanation?” asks Ed Jarzembowski, a palaeoentomologist working at the Maidstone Museum and Bentlif Art Gallery in Maidstone, Kent. “Perhaps they got that big simply because their prey grew larger.” Andrew Ross, curator of fossil arthropods at the Natural History Museum in London, believes there could be other factors at work, such as a lack of predators, or changes in life cycle or climatic factors such as temperature. “We can’t just view it as a simple function of high oxygen levels,” he says.

Besides, says Andrew Watson, a geochemist at the University of East Anglia, the numbers don’t add up. To breathe, dragonflies take in oxygen by diffusion via thin tubes or trachea. But even 35 per cent oxygen will only increase the maximum diffusion distance through the dragonfly’s airways by about 67 per cent. “I can see why they might have got nearly twice as big, but how come they ended up five times as big as their modern cousins?” he asks.

Robert Dudley, an insect physiologist from the University of Texas at Austin, believes he has some answers. “Nobody is saying that high oxygen means everything will get big. It just raises the ceiling, the maximum size that insects can attain,” he says. In terms of maximum size, the important factor is not the wingspan, but the size of the flight muscles, and these are housed in the thorax. Better to look at the diameter of the thorax, says Dudley. Even in giant dragonflies, it is no more than 2.8 centimetres across, compared with 1 centimetre in modern dragonflies.

So are dragonflies sensitive to oxygen levels or not? Because the giants disappeared 250 million years ago, we’ll never know for sure. But their surviving relatives are peculiarly sensitive to oxygen levels. Jon Harrison of Arizona State University and John Lighton of the University of Nevada at Las Vegas have measured the respiratory rate of insects during flight. They have found that most insects are unaffected by changing oxygen levels, but dragonflies do actually fly better if given more oxygen.

Dragonflies depend on an inefficient method of ventilating their airways in which they create draughts by flapping their wings harder. When flying, they can’t get quite enough oxygen, and that takes the edge off their performance. Presumably, say Harrison and Lighton, the reverse would also be true: when oxygen levels are high, dragonflies could get bigger and still fly as well as before. Greater size gives dragonflies a competitive advantage, so they grew larger during the Carboniferous period because the extra oxygen gave them a selective boost.

In fact the denser air of the Carboniferous would have been just the kick that life needed to get airborne in the first place, Dudley suspects. Chronologically it fits. The first flying insects evolved in the early Carboniferous when oxygen levels were rising. And birds and bats evolved in the Cretaceous around 100 million years ago, another period of high oxygen levels.

There is even evidence in the modern world that a high-oxygen environment leads to gigantism. Dudley has begun rearing fruit flies in air at slightly higher pressures and oxygen levels than normal. It is still early days, but even after five generations they are putting on weight, the fifth generation being 15 per cent heavier than the first. “We only see an increase in size if oxygen levels are raised a little at a time, giving the flies the chance to adapt from one generation to the next,” he says. “There’s no change in size if you go straight up to 35 per cent – that actually limits their growth.” And he does not know yet whether these changes occur at the embryonic, larval or adult stages of the life cycle, or whether they are influenced by factors such as population density. “We need to look at exactly how they are adapting,” he says.

His answers will be awaited eagerly, not least because they might tell us something about how to slow the ageingprocess – perhaps even in people. Like most creatures, too much oxygen can be bad for us. Oxygen free radicals, produced continuously in normal metabolism, are thought to be the major cause of human ageing. But more oxygen means a faster metabolism, and so more damage from free radicals. In coping with higher oxygen levels, the fruit flies are effectively deferring their own ageing – and getting bigger and healthier into the bargain. Now Dudley plans to look at which genes they call on to do this.

Creatures swelled by an oxygen-rich diet exist outside the lab too. Oxygen levels vary with the temperature and salinity of water, and are twice as high in cold freshwater lakes as in tropical seas. Gauthier Chapelle of the Royal Belgian Institute of Natural Sciences in Brussels and Lloyd Peck of the British Antarctic Survey in Cambridge decided to test whether these patterns might account for the gigantism of some species of shrimp-like crustaceans known as amphipods, a staple diet of many species of fish such as juvenile cod, which in their turn are eaten by seals.

In cold freshwater lakes such as Baikal in Siberia, they also found that amphipods grow twice as big as their saltwater cousins at the same temperature, and five times the size of their tropical relatives. When Chapelle and Peck plotted the results against dissolved oxygen, they found a nearly perfect fit: oxygen could account for 98 per cent of the variation.

But this raises some immediate issues. If high oxygen levels can breed such giants, they must also be vulnerable to falling oxygen levels. Should global warming continue, then water temperatures will rise and giant amphipods will be among the first species to die out, with devastating consequences for the creatures that eat them. Given the crucial position of today’s leviathans in the food chain, it’s a question worth pursuing. All the more reason to find out more about why those giant dragonflies evolved 300 million years ago, and why they died out.