Oxygen

by Nick Lane

  Perhaps the most surprising feature of all this is that we simply do not know the extent to which high atmospheric oxygen affects the spread

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  of fire in real ecosystems. I understand that trash cans stuffed with wet organic matter are being detonated in high-oxygen atmospheres as I write

  — science marches ever on — but from work published to date we can come to no firm conclusions about whether fire really would have posed an insurmountable problem in the hypothetical Carboniferous atmosphere. Given the devastation caused by forest fires today, it is hard to imagine that so much extra oxygen would not have risked global conflagration, but we must bear in mind two factors. First, most fires today are ignited, either accidentally or intentionally, by people. There would be far fewer fires today if they were ignited only by lightning. If, in the past, the risk of fire was greater, this extra risk might have been counterbalanced by a much lower rate of ignition: fires may have been no more common then than they are today. Second, plants have an extraordinary capacity to adapt to regular devastation by fire.

  Our knowledge of the adaptations of modern plants to fire allows us to scrutinize the fossil record for evidence of similar adaptations in Carboniferous or early Permian times. These issues have been examined in an illuminating and unsurpassed 1989 review by Jennifer Robinson, working at the time at Pennsylvania State University. She argued that if oxygen levels were high during the Carboniferous, we should expect to find adaptations to fire in fossil plants. Conversely, failing to find them would be a good case against a high-oxygen atmosphere. Going one step further, Robinson argued that, while adaptations to fire do not prove the case for high oxygen, a stronger case could be made if even swamp plants adapted to fire in the Carboniferous. This would indeed be curious.

  Today, most swamp plants have no need to adapt to fire, because the fire risk in waterlogged environments at present oxygen levels is virtually zero.

  In her survey of Carboniferous swamp plants, Robinson came to the tentative conclusion that they really had adapted to fire. I say tentative, because there are some difficulties of interpretation. Succulent leaves, for example, might retard the spread of fire, but might also be an adaptation to watery surroundings, or at least an expression of plenty. Deep tubers (along the lines of potatoes) may store enough energy to fuel regeneration of the plant after destruction by fire, but may alternatively be forced on the plant by the depth of the bog. Morphological adaptations are even harder to interpret in plants that have since fallen extinct. Notwithstanding these caveats, however, the fossil record is consistent with the idea of fire resistance. Most large plants at the time had deep tubers, thick bark

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  with a high lignin content, succulent leaves and branches high above the ground, out of reach of any fire that might have swept through the brush-wood. And there were few hanging vines or fronds that would enable ground fire to move into the canopy.

  The appearance of the giant lycopods, the dominant trees of the Carboniferous swamps, is reminiscent of palm trees, although they are not related. The beautiful geometric patterns of their thick, lignin-impreg-nated bark preserve well and are commemorated in some of the ornamen-tal columns at the Natural History Museum in London. Whether or not the giant lycopods were specifically adapted to fire, they would certainly have been hard to burn. Smaller survivors from the era, such as ferns and the horsetail Equisetum, are less obviously fire-resistant, but can also be hard to burn as they contain high levels of fire retardant. In a wry aside, Robinson notes that “modern Equisetum is almost unburnable (personal observation), perhaps due to high silica content.” I can’t resist the image of Robinson as a petulant pyromaniac, stamping her foot in frustration as the horsetails fail to set alight. True science is born from this kind of passion.

  Other aspects of the swamp environment also suggest periodic ravaging by fire, in particular the abundance and properties of fossil charcoal. Some coals contain over 15 per cent fossil charcoal by volume —

  an extraordinary amount if we consider that coal beds are formed in swamps, which under modern conditions virtually never catch fire. The closest modern equivalents to Carboniferous swamps, the swamps of Indonesia and Malaysia, are almost charcoal-free. The discrepancy led many scientists to question whether fossil charcoal was perhaps an impostor — another type of coal not formed by charring at all, but which just happened to look similar. Finally, however, Given, Binder and Hill demonstrated in 1966 that the questionable charcoal really had been exposed to temperatures of several hundred degrees: it really was charcoal and not some form of compressed, unburned coal. Today, few geologists dispute that wildfires once burned frequently in swamp environments.

  What is not agreed is why. It may have been a result of high oxygen, making fire in waterlogged surroundings more likely, or it may reflect no more than the local climate, and the frequency at which the swamps dried out.

  Re-examining the fossil charcoal record from the perspective of variable oxygen throws new light on the conundrum. Coals that formed during periods of hypothetically high oxygen, such as the Carboniferous

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  and Cretaceous, contain more than twice as much charcoal as the coals that formed during low-oxygen periods like the Eocene (54 to 38 million years ago). This implies that fires raged more frequently in times of high oxygen and were not related to climate alone. Some of the properties of the charcoal support this interpretation. The shininess of charcoal depends on the temperature at which it was baked. Charcoals formed at temperatures above about 400°C are shinier than those that cooked at lower temperatures, and so reflect back more of the light directed at them. The difference can be detected with great accuracy using a technique known as reflectance spectroscopy. The shininess of fossil charcoals from both the Carboniferous and Cretaceous implies that they formed at searing temperatures, almost certainly above 400°C and perhaps as high as 600°C, in fires of exceptional intensity. The temperature at which a fire burns, of course, depends on many factors, including the type of vegetation (modern conifers burn at much higher temperatures than deciduous trees), the thermal conductivity of the wood and the height of the water table; but an important factor is the level of oxygen. The simplest explanation for the twin peaks of charcoal reflectance in the Carboniferous and the Cretaceous is that oxygen levels were highest then.

  The fireworks that brought the Cretaceous to an abrupt end support the idea of high oxygen levels. A catastrophic firestorm may have accompanied the extinction of the dinosaurs. One piece of evidence supporting the theory that a giant meteorite hit the earth 65 million years ago is a thin layer of rock rich in iridium that delineates the boundary between the Cretaceous and the Tertiary — the so-called K–T (Cretaceous–Tertiary) boundary. This thin band of iridium-rich rock has now been found at more than 100 sites worldwide. Iridium is rare on Earth, much rarer than gold, but is relatively common in meteorites.6 In fact, the 2 : 1 ratio of iridium to gold in samples from the K–T boundary closely matches that found in meteorites. The presence of iridium in a thin band all around the world suggests that the meteorite shattered on impact, throwing fine dust high into the stratosphere, which later settled out to form the iridium layer.

  6 A competing theory argues that the iridium is derived from the giant volcanic eruptions of the Deccan traps in India. Either event might have produced a catastrophic fire, though it is hard to see how the Deccan traps theory could account for the evidence of extraterrestrial impact on the Yucatan peninsula in Mexico (the shallow seas retreated, leaving evidence of a crater filled in with sediments), or the proposed ‘megawave’ tsunami that followed.

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  In 1988, Wendy Wolbach, then working on her PhD thesis, and her colleagues at the University of Chicago, presented evidence in a paper to Nature that the iridium was mixed with soot at 12 sites from the United States, Europe, North Afric
a and New Zealand. She argued, on the basis of the isotopic uniformity of the carbon, that the soot had been deposited by a single global fire in the wake of the impact itself. Simple calculations suggested that about 25 per cent of terrestrial biomass of the planet had perished in the flames. The headlines at the time were colourful, if predictable, along the lines of ‘Dinosaurs Barbecued in Giant Fireball!’

  Wolbach’s work has found support more recently in other evidence for a great conflagration. In 1994, Michael Kruge and his colleagues at the University of Southern Illinois described a belt of fossil charcoal 3 metres

  [10 feet] thick in Mimbral in northern Mexico, and argued, from its curious cocktail of terrestrial and marine sediments, that terrestrial plants must have charred in a firestorm (ignited by the passage of the meteorite through the skies), then drowned in the deep sea by the backwash from a giant tsunami, or megawave, caused by the impact of the meteorite in shallow tropical seas. While their interpretation has been queried, the evidence for an exceptional fire at the time is hard to ignore.

  If indeed there was such a fire, then a high-oxygen atmosphere may have sealed the fate of the dinosaurs. This is believable, if only because other large meteorites have hit the Earth without causing mass extinctions. For example, a major impact formed the Ries crater in Germany 15 million years ago. The impact threw huge boulders more than 95 kilometres [60 miles] into Switzerland and the Czech Republic, and droplets of molten rock over several hundred miles, but not even the local mammal populations were affected. The Montagnais and Chesapeake Bay impacts formed craters 45 and 90 kilometres [28 and 56 miles] in diameter respectively, but neither brought about a mass extinction. It seems possible that the added zest needed for an explosive doom is a little extra oxygen.

  We now have two independent empirical models — the mass balance and isotope models — which concur that oxygen levels reached 35 per cent during the Carboniferous and early Permian. Also, plants that evolved at the time are resistant to high levels of oxygen; their productivity is barely

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  affected by photorespiration in high-oxygen atmospheres. Fire presents a serious risk in these conditions, but by no means rules out vegetative cover even in dry conditions. Jennifer Robinson, in another of her vivid personal observations, suggests that a modern analogy might be the thinned and locally denuded cover found on bombing ranges in seasonally dry climates. Swamps protect against fire, but even swamp plants of the time show morphological adaptations to fire, including thick, lignin-rich bark, deep tubers and high crowns. Among the survivors from the Carboniferous, some ferns and horsetails have a high content of fire-retardants such as silicate. The environment shows signs of regular wildfires in the form of abundant fossil charcoal, and this charcoal probably formed at the searing temperatures characteristic of high oxygen. There is some evidence that the Cretaceous ended with a catastrophic firestorm.

  Altogether the case is sufficiently strong to have convinced some scientists to return to the old bugbear of insect gigantism. Was that, too, related to high oxygen levels?

  I cited the Dutch geologist M. G. Rutten at the beginning of this chapter. He argued that the primitive means by which insects breathe might limit their size and flight performance. Insects take in air by way of fine tubes or trachea that open directly to the air through pores in the external skeleton and then branch to penetrate every cell in the insect’s body. The idea is that the size of flying insects is restricted by the need for oxygen to diffuse through the tracheal system. Any increase in insect size means that oxygen must diffuse over greater distances through the tracheal system, and so makes flight less efficient. The effective upper limit to passive diffusion down a blind-ending tube (at modern atmospheric levels of oxygen) is about 5 millimetres [1/5 inch]. According to Robert Dudley, a physiologist at the University of Texas, an increase in the oxygen content of the air to 35 per cent would increase the rate of oxygen diffusion by approximately 67 per cent, enabling it to diffuse over longer distances. In other words, air that contains more oxygen allows the minimum amount needed for respiration to reach further into the insect’s trachea. This would improve the oxygenation of flight muscles, allowing thicker constructions and permitting insects to grow larger. While other selective pressures, such as predation, probably drive the actual tendency to get bigger, higher oxygen levels raise the physical barrier to greater size.

  So far so good, but there is one problem with this line of reasoning: the tracheal system may be primitive, but it is far from inefficient — with

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  it, flying insects achieve the highest metabolic rates in the whole of the animal kingdom. Almost without exception, insect flight is totally aerobic, which means that their energy production is dependent entirely on oxygen. In spite of our well-ventilated lungs, powerful hearts, elaborate circulatory systems and red blood cells packed with the oxygen-carrier haemoglobin, we are less efficient. Sprinters cannot breathe in enough oxygen to power their efforts and their muscle cells must instead resort to the less efficient process of energy production by anaerobic glucose breakdown, or glycolysis, which produces a mild poison, lactic acid, as a by-product. The longer we persist in violent exercise, the more lactic acid builds up, until finally we are left half paralysed, even if we are running for our lives. Heavy-legged exhaustion is the product of a respiratory failure that does not trouble insects. If you ever thought that a housefly never grows tired of buzzing, you were probably right: unfortunately for us, it does not poison itself with lactic acid.

  The limits of insect flight are not at all easy to define. In a handful of rather quirky experiments dating back as far as the 1940s, experimenters have tried tethering insects, attaching tiny weights, cutting oxygen levels to a fraction of normal air, and replacing nitrogen with light-weight helium mixtures. All went to show the surprisingly wide safety margins of insect flight. Some insects are even able to fly in low-density helium mixtures with an oxygen content of just 5 per cent. In most experiments, insects gained no apparent benefit if oxygen levels were increased to 35 per cent. The broad conclusion was that insect flight is not limited by tracheal diffusion, so oxygen cannot act as a spur to greater size. This is still the opinion of many entomologists, but the tide is beginning to turn.

  The reason the tracheal system is so efficient is that oxygen remains in the gas phase, where it can diffuse rapidly, and need not pass into solution until the last possible moment, as it enters the flight muscle cells themselves. As a result, the ability of the tracheal system to deliver oxygen typically exceeds the capacity of the tissues to consume it. The only real inefficiency is the blind endings of the trachea, which branch into fine tubules in much the same way as the blind bronchioles in our own lungs.

  Just as we suffocate if we cannot physically draw breath, so too insects are limited by the diffusion of gases in the blind alleys of the tracheal system.

  Most insects get around this difficulty, as we do ourselves, by actively ventilating their trachea.

  For insects, there are two ways of ventilating the trachea, known as

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  abdominal pumping and autoconvective ventilation. Most ‘modern’

  insects, including wasps, honeybees and houseflies, rely on abdominal pumping, in which the insects contract their abdomens rhythmically to squeeze air through the tracheal network. The rate of pumping changes in response to the amount of oxygen available. If honeybees are placed in low-oxygen air, for example, their metabolic rate remains constant —

  they continue to get through the same amount of oxygen as they fly —

  but the rate of water loss by evaporation may increase by as much as 40 per cent, implying that the bees compensate for the low oxygen by pumping their abdomens more vigorously, thereby increasing the rate of tracheal ventilation, and so evaporation. The efficiency of this process allows most insects to keep an even keel in changeable conditions.

&
nbsp; Dragonflies, locusts and some beetles rely on the second, more primitive, means of ventilation — autoconvective ventilation. This is a splendidly opaque way of saying that they create draughts when they flap their wings. Insects that depend on autoventilation can increase airflow in their trachea by increasing the frequency or amplitude of wing beats —

  they flap their wings harder. There is of course a catch here: beating wings demands energy, and the harder they beat the more energy is needed.

  Abdominal pumping requires little energy in comparison. As energy production requires oxygen, and the availability of oxygen can only be increased by beating, which consumes the extra oxygen, dragonflies and other autoventilating insects may be uniquely susceptible to fluxes in oxygen levels.

  In principle, a rise in oxygen levels should enable dragonflies to beat their wings less actively to achieve the same flight performance; or, for a constant rate of beating, the body size might be increased. In a detailed study published in the Journal of Experimental Biology in 1998, Jon Harrison of Arizona State University and John Lighton of the University of Utah put these ideas to the test, and finally produced solid evidence that dragonfly flight metabolism is sensitive to oxygen. They measured carbon dioxide production, oxygen consumption and the thoracic temperature of free-flying dragonflies kept in sealed respiratory chambers.

  Raising the oxygen content from 21 to 30 or even 50 per cent increased the metabolic rate. This means that, in today’s atmosphere, dragonfly flight is limited by oxygen insufficiency. If dragonflies can fly better in high-oxygen air, then presumably larger dragonflies, which could not generate enough lift to become airborne at all in today’s thin air, would have been able to fly in the postulated oxygen-rich mix of the Carbonifer-