Why Were Carboniferous Insects So Big? Dragonflies With the Wingspan of a Gull

The Carboniferous, from 359 to 299 million years ago, was the age in which forests first covered the continents. Trees had evolved lignin, the tough polymer that lets wood stand up, and the fungi and bacteria that could break lignin down had not yet caught up, so that dead trees did not rot but piled up in swamps, were buried and became the coal seams that name the period. Every tree that was buried rather than decomposed was carbon taken out of the air and oxygen left in it, and over tens of millions of years the balance shifted: carbon dioxide fell to levels near today's and oxygen rose to something like 30 to 35 percent of the atmosphere, against 21 percent now. Fires burned in air that rich even when the wood was wet, and charcoal from the period is found in quantity.

Insects do not breathe with lungs. Air enters through holes along the body, the spiracles, and diffuses down branching tubes, the tracheae, directly to the tissues, and diffusion is slow over distance. The tubes must be wider and take up more of the body the larger the animal is, until in a big insect there is no room for anything else, which is why the largest insects alive, a stick insect of 60 centimetres and beetles of 100 grams, are near the limit that today's air allows. Raise the oxygen and the same tubes deliver more, so the limit rises, and the giants of the Carboniferous are what a body plan with a fixed ceiling does when the ceiling is lifted. The evidence:

• •The largest insects in the fossil record coincide with the oxygen peak reconstructed from the chemistry of ancient soils and sediments, and shrink as it falls
• •Modern insects raised over several generations in oxygen-rich air grow larger, and dragonflies raised in low oxygen grow smaller, in laboratory trials
• •The tracheae of large modern beetles take up a share of the body that is close to the maximum the animal could afford, as X-ray imaging shows
• •Denser air, which the extra oxygen also produced, made flight easier for a large wing

Meganeura and its relatives, the griffinflies, were not true dragonflies but an earlier order built the same way, with two pairs of wings, huge eyes and grasping legs, and they were the top aerial predators of the swamps, hunting other insects and perhaps small amphibians; the largest, Meganeuropsis, from the early Permian of Kansas, had a wingspan of 71 centimetres. Arthropleura was a millipede with dozens of pairs of legs whose trackways, half a metre wide, are found in Nova Scotia and Scotland, and whose diet was probably the litter of the forest floor; a 75-centimetre section found on a Northumberland beach in 2018 belonged to an animal about 2.6 metres long and 50 kilograms in weight, the largest arthropod that ever lived on land. Pulmonoscorpius, a scorpion of 70 centimetres, and Mazothairos, a mayfly relative with a 45-centimetre span, filled out a fauna in which the vertebrates were still mostly small amphibians.

The oxygen fell through the Permian as the coal forests died back and the fungi learned to digest wood, and the giants went with it, the last of the great griffinflies vanishing in the Permian and the largest insects of the Triassic being ordinary in size. A second cause arrived in the Jurassic: birds, and before them the pterosaurs, which hunted large flying insects and favoured the small and agile, and a study of insect wing sizes across 150 million years found that the trend with oxygen breaks down exactly when birds appear, after which insects shrink whatever the air does. The largest insects now are the ones that do not fly much and live where birds are few, and the dragonfly at the pond, with its ten-centimetre span, is the shape the giants took when the air thinned and the sky filled with things that ate them.

Carboniferous insects grew to the size of gulls because the coal forests, whose wood nothing could yet rot, buried carbon and pushed atmospheric oxygen to around a third, and insects, which breathe by diffusion through tubes, can only be as large as their air allows. Griffinflies of 70-centimetre span, two-metre millipedes and giant scorpions filled the swamps, and they shrank as the oxygen fell in the Permian and disappeared for good when pterosaurs and birds began eating the large and slow.