There’s one other advantage, perhaps, to evolving small body size and migrating deep into insulating blankets of moist soil. The Devonian period, with the evolution of plants with leaves, saw the first accumulations of leaf litter, and consequently the first wildfires. Charcoal deposits from the Devonian document that fires emerged with the first forest communities. With each fire the dry layers of leaves would be burned away, and communities of larger arthropods would recolonize the area. Small arthropods living in the deeper moist soil would be insulated from such local catastrophes.
Springtails Vault to Devonian Superstardom
Probably the most important fossil beds of Devonian-age hexapods are the Rhynie cherts of Aberdeenshire, Scotland. The fossils at Rhynie were formed between 396 and 407 million years ago, when present-day Scotland was a low-lying marsh located in the tropics. Hot spring activity at the Rhynie marsh produced crystal quartz called “chert,” which preserved some very small organisms with remarkable clarity; fossil plants from the area, for instance, are preserved in cellular detail. The Rhynie cherts also contain the oldest-known fossils of mycorrhizal fungi, but Rhynie is famous for another reason: among the fossils are the oldest examples of well-preserved hexapods, Rhyniella praecursor.4 Rhyniella is also the oldest example of a soil hexapod that continues to thrive in the modern world: the order Collembola, known as springtails.
Apparently the first hexapod group to successfully colonize the finest niches available in microbial soils, springtails get their common name from the fact that they possess an unusual forked taillike structure on the abdomen that allows them to pole vault up to twenty times their body length and spring themselves to safety when disturbed. Springtails are extremely small, ranging in size from only one to ten millimeters long, and they can be exceedingly numerous: their populations commonly number in the thousands per square meter of soil surface. There are records of as many as a hundred thousand springtails per square meter of soil surface in some remote island shorelines, where there may be fewer predators. Some springtails prey on bacteria, nematodes, tardigrades, rotifers, and protozoa, but most of them scavenge on organic plant materials. Despite their small size, they still account for high levels of arthropod biomass, and because springtails are among the commonest soil micro-arthropods associated with decomposing organic materials, they doubtless contributed in a serious way to the processing of Devonian soils. Their feeding speeds the recycling of nutrients from decaying plants, and their activities improve the physical characteristics of soils, improving nutrient flow and drainage.
FIGURE 4.1. Springtails (order Collembola) are the most diverse six-legged arthropods inhabiting forest soil and leaf litter. Despite their microscopically small size, they are often numerous and important nutrient recyclers, and sometimes they are quite beautiful. (Photo by Kenji Nishida.)
Springtails share the same indirect reproduction methods with their myriapod ancestors—male springtails produce spermatophores, which they post on stalks in their moist, mossy environment—and their mating rituals may seem comical to us. Some males spend a lot of time posting stalked spermatophores in a circle around a female, in high hopes that she will pick up at least one, only to see her pole vault away, out of the circle of love. Other male springtails have evolved clasping antennae that allow them to grab onto a female and ride around with her, hopefully until she becomes more receptive. These primitive mating methods would seem to limit the springtails to moist environments, yet modern springtails have evolved to survive under some surprisingly extreme conditions. Some have glycol antifreeze in their blood, and they are the only hexapods known to live along the shorelines of Antarctic islands. On the other extreme, some have evolved to survive in desiccating deserts. They can dry out but rehydrate when it rains.
Because springtails, along with other kinds of ancient wingless hexapods, are microscopically tiny, people rarely notice them. If you want to find them for yourself, there is actually a very simple sampling method, called a Berlese funnel, which takes advantage of their dislike of dry conditions. You can easily and cheaply fashion one of these at home. All you need is a large plastic funnel (like you might use for adding antifreeze to a radiator), some window screen, a jar, some alcohol, and a desk lamp or utility light. Cut a round piece of screen and place it in the bottom of the funnel. Set the funnel on top of a large jar with some alcohol, and add to the funnel a sample of moss, leaf litter, soil, or any such material likely to contain microscopic arthropods. Usually a scoop of any material from the forest floor will work well. Place the light above the wide end of the funnel, close enough to cast some heat and light on the sample, but not close enough to start a fire. As the moss and soil dries, the tiny arthropods will migrate downward to the bottom of the sample. When they get to the screen (if the mesh is not too small) they will fall through, into the alcohol jar. This simple method is one of the easiest ways to see a diversity of springtail species, and may be the only way most of you will see the other kinds of rarer hexapods discussed in the remainder of this chapter.
A Tale of Tails
Other kinds of primitive hexapods survive in the order Diplura (the diplurans). The name literally means “two tails” and refers to the two prominent taillike cerci that extend from the end of their abdomens. The diplurans are considered to be closely related to the springtails (they share a unique mouthpart structure—the mandibles are withdrawn into a pouch in the head), but unlike the collembolans, they are scarce and rarely encountered. The only place I have commonly seen living diplurans is in the moist cloud forests of eastern Ecuador, where they, along with numerous springtails, inhabit the dense mosses and soil layers that coat tree trunks and large tree branches, often high above the ground. Moreover, the fossil record of Diplura is very poor, which is hardly surprising since they are soft-bodied and live only in very moist and fungus-ridden microhabitats. Nevertheless, we know quite a bit about their anatomy and biology based on studies of several living species. Less specialized than that of a springtail, their body form is about as simple as it gets for hexapod arthropods: a head with multisegmented antenna and mandibles but no eyes, a thorax with six legs but no trace of wing development, and an elongate multisegmented abdomen ending with a pair of cerci. Diplurans come in two forms, depending on the shape of the terminal cerci. Some have long multisegmented cerci that look like antennae coming off the tail end, and they use them as back-end “feelers.” These species all seem to scavenge organic debris and fungi in soils and mosses. The other kinds of diplurans have cerci whose segments are fused into forceps-like pincers. Many of these species appear to be predatory and some are known to capture small prey, such as springtails or small insects, with their pincerlike “tails.” Like other kinds of very primitive hexapods, dipluran adults continue to molt their exoskeletons after they reach sexual maturity and adulthood, and some species are known to molt up to thirty times.
FIGURE 4.2. The two-tailed diplurans (order Diplura, family Campodeidae) are reclusive hexapods living in moss and leaf litter, which are seldom seen by humans. (Photo by Kenji Nishida.)
Among other primitive six-legged animals thought to have evolved in the Late Devonian are the jumping bristletails, or, simply bristletails. As the common name implies, they have long bristly tails, and they can jump by arching their body. Their scientific name, the order Archaeognatha,5 means “ancient mouth” and refers to their very simple jaw, which is hinged on only one weak point, at the lower head. These jaws are sometimes called milling mandibles, presumably because they can only gently grind food. Bristletail remains have been found in the Devonian Gilboa forest of New York, but several species of these ancient hexapods survive even today in moist forest soils and along shorelines near the oceans. Unlike most modern insects, they are unusual in having abdominal appendages called styli, which may be remnants of ancient leg parts. These living fossils have a few tricks of their own. They use their own feces to glue their bodies to the ground when they molt. This apparently allows them to more successfu
lly pull themselves from their old skeleton during the molting process; however, if the glue fails, they can’t get out of the old skeleton and they die. It’s an indication that early insects needed to evolve efficient molting methods.
FIGURE 4.3. Jumping bristletails (order Archaeognatha) are among the most primitive of living insects. Unlike most insects, they have appendages (styli) on their abdominal segments. (Photo by Kevin Murphy.)
Modern entomologists divide the hexapods into two groups depending on whether the mouthparts are withdrawn into a pouch, as in springtails and diplurans, or clearly exposed, as in most other hexapods. By this criterion, the true insects include only the hexapods with exposed manibulate mouthparts: the bristletails, their relatives, and all their descendants. Perhaps the oldest undisputed fossil of a true insect is that of Rhyniognatha hirsti, also found in the Rhynie chert formations and aged at 396 to 407 million years old. Although based on little more than a fossil tooth, this organism is particularly intriguing because it has a double-hinged mandible with two hinge joints called condyles, just as in most modern insect species. This type of jaw could belong to a wingless insect like a silverfish or firebrat, placed in the order Zygentoma (formerly Thysanura). However, all flying insect species evolved from ancestors with a double-hinged mandible. This has led some scientists, such as Michael Engel, to speculate that insect flight may have arisen much earlier than previously thought, perhaps as early as the Devonian. Although there are no fossil wings to validate this claim, it is a reasonable possibility. Further, if insects with such refined body plans had indeed emerged by the Late Devonian, then it leads to further speculation that the six-legged body form may have also evolved earlier than usually supposed and that perhaps insects first lived during the Late Silurian. Such thoughts must remain speculative for now, pending the discovery of new fossils that might push the date of the earliest insect back even farther in time. What we do know for sure is that true insects had evolved during the Devonian period, and the terrestrial ecosystems that they emerged in were present at least since the Silurian.
During the Late Devonian, 360 million years ago, complex forest communities of treelike plants had emerged and were widespread across moist tropical lowlands. In the deeply shaded soils below, under thick layers of accumulating leaves, there lived abundant communities of small six-legged scavenging arthropods, including springtails, jumping bristletails, and silverfish. The planet had become buggy. These crawling organisms would seemingly be content to stay in the comfort and safety provided by the soil, the leaf litter, and other mossy, humid habitats. Yet at the end of the Devonian, and onward into Carboniferous times, the world again changed dramatically. At the end of the Devonian the planet cooled somewhat, glaciers formed, sea levels dropped, and the marine reef community experienced mass extinctions. On land, the composition of plant communities drastically altered into the Early Carboniferous period. But the most dramatic change, perhaps, is the first appearance of flying insects during the later part of the Early Carboniferous. By the second half of Carboniferous times, about 320 million years ago, the earth’s forests were forever transformed into a fairyland of glimmering and fluttering wings. The next part of the story, the tale of insect flight origin, is one of the most important turning points in the history of life. Where in the world did wings come from?
5
Dancing on Air
In more than 600 million years of animal evolution, there have only been a handful of novel features, such as the wings of insects, that seem in our ignorance not to be mere modifications of something that came before.
DOUGLAS J. FUTUYMA, Science on Trial
I have an enduring obsession with wings and flying things. There are few sights more fascinating for me than watching an insect in flight and few tasks more challenging than pursuing one. For as long as I can remember I’ve been particularly intrigued by the more colorful flying creatures like butterflies and moths, but I don’t think that I’m the only one. Judging from the growing popularity of butterfly houses and insect zoos, it appears that most people gain pleasure from the sight of butterflies in flight, even those who detest other sorts of insects. There is a magical, almost fairy-tale quality to them. Is this because we’ve seen too many Disney movies with delicate little fairies set with insect wings? Or do cartoonists draw fairies with insect wings because dragonflies and butterflies occupy a magical place in our psyche? I doubt anyone would enjoy the fairies so much if we depicted them with bat wings or fish fins.
I’ve been observing insects for fifty years, but one recent June I witnessed a truly magical event, the likes of which I’d not seen before. My family and I were visiting relatives at their cottage on Canada’s Lake St. Clair. We were enjoying a Father’s Day barbecue, and by coincidence massive numbers of Heptagenia mayflies, which had emerged from the lake overnight, were covering all the trees, the bushes, and the cottages. I’d seen this phenomenon several times before, as a child visiting lakeshores in northern Michigan, but never anything of this magnitude. In the evening, as the sun set orange and fiery over the lake, they rose, shimmering, by the thousands, by the millions, and engaged in a frenzied mating dance. Vast mayfly clouds soared along the shorelines as far as they eye could see, extending ten to fifty feet above the ground, to about fifty feet over the lake. The density of insects was so great that, standing below a swarm and looking up, I could hardly see the sky. Just within my field of view, several million mayflies, mostly males, were dancing in the twilight, slowly rising up and drifting back down in undulating waves. Swarming is a male tactic, a visual display for attracting virgin females from a distance.1
Dance ’til You Die
Modern mayflies are truly ephemeral creatures. Since their young nymphs breathe using platelike tracheal gills, they require very clean, cold freshwater for their survival. Because of recent human-induced waterway pollution, massive emergences of many species are increasingly less frequent. Even so, aquatic mayfly nymphs, also called naiads, spend most of their lives hidden in the bottom sediments of freshwater lakes, marshes, and streams, where they feed on algae and organic debris and develop gradually. Once a year, often in synchrony, they emerge from the water, molt, and develop wings from their nymphal wing buds. The adults then have very short lives; many live for less than one day.
Examples of paleopteran insects (a term that means “old wings”), mayflies are among the oldest surviving insects with the most ancient sort of wing design. If you get a chance to see a mayfly, take a close look. You’ll observe a relict that developed flight about 330 million years ago in the Carboniferous times. Like most insects, mayflies have four wings: a front and a back pair located on the middle and last segments of the thorax. The front wings are much larger than the back ones, and provide most of the lift for flight. All four wings are simple, however, in that they are capable of moving only up and down; mayflies don’t have the ability to flex and twist their wings at the base, as most modern insects are able to do. A mayfly’s wing is a delicate membrane overlaying a complex supporting network of many fine veins. Mayflies share this high number of veins with the earliest known flying insects from the later half of the Carboniferous (the Pennsylvanian subperiod). They have another odd feature that is considered to be very primitive: after emerging from water and developing wings, they do not fly right away. Instead, mayflies go through a subadult molting stage with functional wings. After one day they molt again, into adults. They are the only living insects that molt after their wings develop, so if you see a winged insect other than a mayfly, you know you are looking at an adult.
FIGURE 5.1. A small mayfly, Baetis magnus (order Ephemeroptera). Mayflies are considered to be the most primitive living examples of flying insects. (Photo by David Rees.)
When mayflies fly, they do so mainly to reproduce. By synchronizing their swarms, however, they are able not only to attract and meet mates but also to swamp predators. Mayflies are not very strong or adept fliers. They can do little more than flutter their wings and
drift and glide in easy patterns. Birds catch them easily, and fish eat their fill as the mayflies land on water. Yet all the predators in the neighborhood can’t make a dent in a mayfly swarm. When a virgin female flies into the disco-dancing cloud, she is quickly grabbed by a long-legged eager male, who transfers a spermatophore. Immediately after mating, the female flies back to the lake, then lands and floats on its surface. If she is lucky enough not to be eaten by a fish, the mother mayfly quickly dumps her eggs into the water as she dies. The eggs sink to the bottom and the cycle of death and rebirth is repeated, just as it has been for 320 million years.2
When mayflies first fluttered over ancient marshes, the skies were an open frontier: there were no birds or other vertebrates to chase them in the air.3 But the Carboniferous freshwaters were home to many species of jawless fishes and amphibians. If mayflies returned to streams and ponds to lay eggs, many were probably eaten, so even then natural selection would have favored synchronized emergence as both a predator-swamping and a mate-finding strategy. I’d like to imagine that even Carboniferous mayflies danced in large clouds to reproduce.
Planet of the Bugs: Evolution and the Rise of Insects Page 9