Although the mayflies and dragonflies are the only surviving insects with this ancient flight mechanism, when it first evolved it was the latest and greatest innovation in animal locomotion. Without any competition from birds, bats, or flying dinosaurs, the old-wing insects took to the air in prolific numbers, and by the Late Carboniferous, the earth’s wet tropical forests were populated by a startling array of flying insect species, almost all of which are now extinct. One of the most notable examples is the order Paleodictyoptera, the old net-winged insects. As the name implies, these insects had a netlike profusion of veins along their old-style wings, which they held out to their sides and were incapable of folding back over their body. But the old net wings conquered the air more profusely than most other insects of the time. Over the Late Carboniferous and continuing through the Permian years there arose a dynasty of paleodictyopteran insects that diversified into at least seventy-one genera, classified into twenty-one families. Some of these species were quite enormous, the largest being about fifty-six centimeters in wingspan (about twenty inches across). They were positively gigantic compared to ancestral flightless insects, clearly indicating that the old net wings had successfully managed to escape the earthbound predators on the forest floor and specialize in tree dwelling, making them some of the first arboreal insects. In the future, most insect species would evolve to live in rain forest canopies.
Part of the old net wings’ success stemmed from their invention of a unique mouthpart style. The oldest known true herbivorous species, they were the first flying insects to evolve piercing and sucking mouthparts (beaks) capable of liquid feeding and tapping into the more nutritious plant parts in ways that no other animal group had done before. Species with long beaks and their nymphs could feed on plant tissues and fluids by piercing soft foliage or tapping directly into xylem and phloem. Other paleodictyopteran species with shorter, broader beaks fed by piercing the developing reproductive cones of ancient plants, and sucking out the liquid, spores, and ovules.
We know that the old net-winged insects fed on various plants, including pteridosperms, cordaitealeans, lycopods, and conifers, because we’ve found fossilized Paleodictyoptera with spores and pollen in their mouthparts and guts. We’ve also found fossil plant remains that show piercing-and-sucking feeding damage, no doubt paleodictyopteran handiwork. They were the only insects around with the right kind of equipment able to make those marks.13 The first plant galls, fossils of deformed plant growth of the kind usually caused by arthropod feeding, also date to the Late Carboniferous. We can’t be sure what insects made these galls—they could have been formed by mites—but they’re possibly the first evidence of insects concealing themselves while feeding inside plants. We also have fossil coprolites, literally fossil insect poop, which contains plant spores.14
Many of the paleodictyopteran insects had pigmented patterns on their wings. These species are preserved in detail in some fine sedimentary compression fossils, and although we don’t know the colors of the wings, we do know that they often had boldly contrasting stripes or spots. What might these markings mean? The most likely explanation is that they provided visual cues for mate recognition, just as in modern dragonflies, grasshoppers, and butterflies. But insects evolve colors for several reasons. It’s possible that some of their pigments might have been cryptic. It’s difficult to know what sorts of leaf markings or color tones might have been prevalent in the foliage of Carboniferous rain forest canopies, but if paleodictyopteran wings were blends of greens, tans, and yellows, the insects may have been highly camouflaged when resting on tree trunks or in foliage. They may well have escaped entirely from the amphibians on the ground, but they may still have had to contend with the tree-climbing scorpions, spiders, and centipedes. Another possibility is aposematic warning coloration. Many modern insects gain toxic defenses by feeding on toxic plants and develop warning colors in their wings to advertise this to predators. Without any birds, this seems less likely to develop, but paleodictyopterans may still have faced an occasional amphibian on low vegetation, tree trunks, or mossy branches. So there might have been selection pressure to develop bright warning colors, even then.15 Another possibility is storage excretion metabolism: some insects shunt nitrogen wastes out of their body tissues by packing them into wing pigments (yellow butterflies are the best-known example). Paleodictyopterans might well have had bright yellow or orange colors in their wings, even in the absence of plant toxins or vertebrate predators. The point I wish to make is simply this: the Carboniferous world had pattern, color, and beauty. The orthodox reconstructions of that ancient period overlook this. I’ve seen several museum panoramas of coal-age swamps, and they always depict a cloudy, drab, green and brown world, usually with a spider, giant dragonfly, and maybe a roach. They never show you the paleodictyopteran insects. I prefer to think that above those swamps flew a shimmering fairyland of multicolored insects, many of which we would certainly consider to be beautiful.
FIGURE 5.2. Fossilized paranotal lobes and patterned front wings of an extinct upper Carboniferous paleopteran insect Homoioptera gigantea (order Paleodictyoptera). (Photo by Olivier Bethoux. © MNHN–Olivier Bethoux.)
My, What Big Wings You Have
The old net-winged insects may have succeeded magnificently by escaping most of the terrestrial predators in the forest understory, but they still had to contend with airborne insect predators, such as the so-called giant dragonflies, or griffenflies, of the now-extinct insect order Protodonata. Among the most spectacular animals of the Late Carboniferous years, the griffenflies were not really true dragonflies but rather a group that resembled them. Members of one of the griffenfly families—of the tropical family Meganeuridae—are the largest insects that ever lived. During the Permian times, Meganeuropsis permiana developed wingspans of seventy-one centimeters (between two and three feet wide), while most other meganeurid species typically had wings four to thirteen inches long. These dragons of the air had sharp, powerful mandibles and spiny front legs for grasping prey. They may not have been really fast or adept fliers, but they were easily able to grab fluttering paleodictyopterans, swarming mayflies, and other flying insects out of the air. They probably also picked off paleodictyopteran nymphs and adults feeding on prominent canopy stems. In the absence of birds, bats, pterosaurs and other flying vertebrates, these Paleozoic giant griffenflies were the dominant predators of the skies, and they were likely the main source of predatory selection pressure shaping the evolution of wing patterns and colors in Carboniferous and Permian insects.
Some researchers have pointed out that the appearance of gigantic flying insects correlates with peaking atmospheric oxygen. Levels had remained around 15 percent from the Cambrian to the Devonian, rising significantly to around 35 percent in the Late Carboniferous. Then they dropped back to about 15 percent by the end of the Permian. Since the times of highest oxygen do correspond to the era of giant flying insects, it is tempting to relate the two. Scientists have suggested that such large insects needed heightened levels to operate their huge flight muscles, and there is some evidence that they had enlarged tracheal systems. Carbon dioxide was also elevated at the start of the Carboniferous but dropped dramatically over the Permian years to nearly modern levels. So it’s also been suggested that the air was thicker and more viscous then, making flight somewhat easier.
These physiological arguments may have some problems. They assume that since oxygen reaches insect cells by diffusing from their tracheal network, a respiratory constraint is placed on the insects’ upper size limit. But it’s important to note that insects can force air through their tracheal system and pump it to cells deep in their body, by contracting their abdominal segments. Also, we don’t know what the giant griffenflies’ metabolic requirements really were. They were the top predators, and nothing else was chasing them. Prey like mayflies and paleodictyopterans probably fluttered along slowly, so there is no reason to assume that the giant meganeurids flew very fast. If they had a slow, lazy flight
pattern, they may have required less oxygen than some large modern insects, like hawk moths. Another thing to consider is that modern dragonflies are very lightweight, and the giant meganeurids probably were as well. Most of a dragonfly’s body is very slender, and it has lots of gas-filled tracheae, which helps a dragonfly to both float on water while laying eggs and to fly more easily. Moreover, there are no modern insects quite so large in wingspan, but there are some massive ones. The heaviest adult insect, the goliath beetle of Africa, can weigh up to a hundred grams. Its thorax is thicker than that of a giant dragonfly, and one of these beetles probably weighs as much or more than a meganeurid air dragon. And goliath beetles can fly just fine, even with the modern atmospheric oxygen level of around 21 percent.
FIGURE 5.3. A gigantic fossil wing of Meganeuropsis permiana (order Protodonata) from lower Permian rocks found in Oklahoma, about 280 million years old. The length of this wing is about thirteen inches. (Photo by Frank Carpenter. Museum of Comparative Zoology, Harvard University. © President and Fellows of Harvard College.)
Oxygen might have been a factor spurring the evolution of the air dragons’ large size, but it probably wasn’t the only one. It’s important to remember that insects develop by periodically molting their external skeleton. So for any insect to grow as large as a griffenfly, it would need to go through a series of progressive molts, and during each one it would be extremely vulnerable to predators. The growth of any giant insect therefore requires that the young live in a largely predator-free environment. Where, then, did young giant griffenflies grow up? We suspect that the immature forms were freshwater aquatic nymphs that breathed with gills (like those of modern dragonflies) and were predators who fed in marshes and ponds,16 where they would have found abundant food in the form of mayfly nymphs or insects that fell on the surface. Like modern dragonfly nymphs, they probably also fed on fish and amphibian eggs, small fish, and amphibian tadpoles. Consider the situation in the Carboniferous years: jawless freshwater fish were spreading to inland lakes and ponds, but the air dragons held the advantage. Because they could fly, the females were able to move inland more easily than fish and occupy temporary ponds and marshes that the fish could not as easily colonize. Griffenflies could also fly inland to unoccupied ponds, ahead of the fish, which, when they finally did arrive, would be attempting to lay eggs in ponds already full of vicious meganeurid nymphs. The large nymphs of many modern dragonflies are able to cover themselves in sediment and debris, and maybe the meganeurids could don similar disguises. Perhaps, as they grew ever larger, they burrowed into soft bottom sediments to complete their molts. If they lived in ponds, the liquid environment would have facilitated their multiple transitions. They would have emerged only to finally molt into fully-winged adults; then they could fly to the comparative safety of the forest canopy, where their main enemies might have been each other.
A New Twist on an Old Style
During the Late Carboniferous, the giant griffenflies started chasing a new kind of insect that was tasty but harder to catch than the old net-winged ones. Neoptera, or the new-winged insects, were faster flyers, and they had an original trick made possible by tiny articulating skeletal plates, called axillary sclerites, in the membrane near their wing base. These allowed directional wing movements that were never possible among the paleopterans. When neopteran insects landed on a plant and were done flying, they could twist their wings at the base, fold them back over their body, and put them away, making the neopterans much smaller than the older insects, which held their wings constantly outstretched, kitelike. This neat twist would open myriad new possibilities for future insect evolution by allowing front and back wings to specialize separately. It made the future evolution of stoneflies, grasshoppers, bugs, beetles, lacewings, butterflies, bees, flies, and most other modern insects possible.
FIGURE 5.4. Fossil folded front wings with eyespot-like markings of an extinct upper Carboniferous neopteran insect, Protodiamphipnoa gaudryi. (Photo by Olivier Bethoux. © MNHN–Olivier Bethoux.)
Some of the neopterans were fast on their feet, too. Quickly after landing, they would deftly fold their wings and run under a leaf or into cracks and crevices, making themselves tough targets for the air dragons. This was such a successful adaptation that before you could say “cockroach,” the tropical world was infested with them. Several groups of new-winged insects appeared during the Carboniferous, but the roaches (order Blattaria) were by far and away the most successful of the age. By the Late Carboniferous there were more than eight hundred species, and they made up about 60 percent of the known Carboniferous insects. They were a bit different from modern species: they could actively fly and females had an egg-laying device, an ovipositor, that resembled a tail. We still classify them as roaches, however, and in terms of species diversity, we should probably call the Carboniferous period the “age of roaches.”17
Roaches have a bad reputation, mostly because of a few bad eggs: a few nasty pest species that overrun our houses and apartments. But please don’t base your overall impression on just those few. Modern tropical forests contain thousands of cockroach species, which enjoy a wide variety of habits. Most live on the ground in leaf litter or under logs, but many live on tree trunks or in the forest canopy. Some are blind and live in caves, while others are semiaquatic and live alongside streams or in bromeliad water tanks high in the treetops. Most are nocturnal, but some are active by day, and some even prefer bright sunlight. The night-active species may stir at different times: some in early evening, some around midnight, and others before dawn. Modern roaches are moderately omnivorous, and they play an important role in the decomposition and nutrient cycling of leaf litter and organic material on tropical forest floors. Several living cockroach species are even known to pollinate tropical plants.
Many of the early cockroaches are thought to have preyed on small soft-bodied insects or scavenged the bodies of dead insects, probably of fallen titanic air dragons. Based on the abundance of fossil fecal droppings, many others are known to have been detritivores, and, like modern roaches, are thought to have played a valuable role in the rapid decomposition of leaf litter. The wood roaches evolved a symbiotic relationship with their gut microorganisms and became the first effective macroconsumers of dead wood. The roaches in turn were the most abundant food source for a host of predators, including scorpions, spiders, centipedes, fish, amphibians, reptiles, and the flying air dragons. So with the onset of roaches an important turn occurred in the cycling of organic molecules. More biomass from plant material escaped the geological cycle of sedimentation and rock formation, and was cycled back into the living world by small animals. The great coal age was coming to an end.
In the Late Carboniferous, around 299 million years ago, the sun rose over moist lowland rain forests of giant horsetails, seed ferns, and ancient conifers. As steam rose from the marshes, scurrying roaches folded their wings and nestled into the leaf litter. In the forest canopy, colorful old net wings basked in the early morning sunlight, absorbing heat and fluttering into the air. Giant shimmering gossamer-winged air dragons lifted to the chase. Down below, in the still-shaded shorelines, the amphibians glanced wistfully to the treetops and worried about their next meal. Along the shorelines, also basking in the morning sunlight, was another new animal, one I haven’t mentioned yet. During the Carboniferous, the lizard-like vertebrates evolved, and by the end of the period there arose large reptile species that ate meat, mostly from fish and amphibians. But you can bet that small ones liked to eat insects whenever they could get them. You can also bet that whenever there was a massive mayfly emergence, all the amphibians and reptiles would be busy lapping up their fill off the low vegetation.
As hungry reptiles patrolled the margins of the coal swamps, the Carboniferous times were waning. The world was getting drier, and while the coal swamp lands were decreasing, conifers were evolving and transforming the terrestrial landscape. Insects had evolved some of their most important traits—wings and the ability to fl
ex them in a complex way—but now that the Permian times were approaching, some even more startling innovations were developing. During the Permian the giant fin-backed reptiles dominated the shorelines, the flying insects diversified like never before, the most gigantic insects of all time patrolled the airways, and complex metamorphosis became widespread. But the Permian is crucial to the history of life on earth not just because of its evolutionary innovations. The end of the Permian marks the biggest change that life has ever seen: a catastrophic mass extinction greater than any before or since. Understanding that event, and why many insects survived it, may prove to be the most important key in explaining why insects rule the planet.
6
Paleozoic Holocaust
The end-Permian mass extinction had the greatest effect on the history of life of any event since the appearance of complex animals.
Planet of the Bugs: Evolution and the Rise of Insects Page 11