1.

The invention of the microscope revealed wonders to the world, and permitted Jonathan Swift to quip:

So, naturalists observe, a flea
Hath smaller fleas that on him prey
And these have smaller still to bite ’em
And so proceed ad infinitum.

By the late twentieth century fascination with the minuscule had begun to pall, and now it takes an exceptional book indeed to reawaken our interest. Thankfully, in David Attenborough’s Life in the Undergrowth, Piotr Naskrecki’s The Smaller Majority, and Jeffrey Lockwood’s Locust we find three works that do so.

Life in the Undergrowth is Attenborough’s tribute to the terrestrial invertebrates. They are, he says, a group of creatures that make life possible for us—whether as scavengers, aerators of soil, or agents of pollination, to name only three of their functions—but because they are small we largely ignore them. As he succinctly puts it, “We are greatly prejudiced by our size.” This is the latest in a series of projects combining television and print in a unique manner that has become Sir David’s métier. His investigations encompass disciplines as diverse as paleontology, botany, zoology, and ethnography; and each is similar in scope to a doctoral dissertation. While most of us think of Attenborough principally as a television presenter, he is also one of the greatest ecologists, synthesizers of evolutionary science, and teachers of our age.

In each of his investigations Attenborough takes multiple parts, including instigator, researcher, scriptwriter, presenter, and author of a book summing up his inquiries. Because of the highly sophisticated recording equipment and laboratories at his disposal, and because he and his team spend long months in the field, fundamental discoveries have been made during the course of this work. Life in the Undergrowth was no exception, with Attenborough’s sound recordist discovering that certain caterpillars create sounds that charm ants into caring for them.

The land-dwelling invertebrates (animals without backbones) are so diverse that they make up most of the species on Earth. This makes producing an overview of them particularly challenging. Attenborough adopts an evolutionary approach, and as he tells his tale he picks out species that take a particular adaptation or behavior to an extreme. This allows him to capture the general direction of the group’s evolution as well as its breadth of diversity, without drowning us in detail.

Life in the Undergrowth commences with the descendants of the first creatures to clamber out of the water and onto land—the scorpions and their relatives. They made the transition some 400 million years ago, long before plants or our ancestors left the oceans. If you have never thought of scorpions as remarkable, Attenborough advises that you try to pick one up, perhaps with a pair of very long forceps. Whichever method you use it will not be easy, for scorpions possess advance warning systems that sense where you are and what you are doing. Their six pairs of eyes are strategically positioned so as to leave no blind spot, and while lacking sharp focus they are capable of detecting the tiniest variations in brightness—and thus movement. Yet they cannot be dazzled because each one has its own built-in “sunglasses,” composed of pigment granules, which cover the lens as light increases.

Before it sees you a scorpion will either have “heard” you through the minute hairs on its claws, or detected your advance through a slit-shaped organ on the upper part of each leg, which is so sensitive to vibration that it can pinpoint the footfall of a beetle a yard away. Or perhaps it will have detected you with its pectines. These comb-like organs have no parallel among other living creatures. They are packed with nerve endings and are probably capable of smelling or tasting minute traces of chemical compounds in the ground over which the scorpion passes.

When a male scorpion meets a female scorpion, his mind is very much on the ground under his feet. You can tell this from his pectines, which scan the earth while he shakes his body back and forth. He then approaches the female and stings her on the soft flesh in the joints of a pincer. This seems to relax her, allowing him to grasp her claw in claw, bring her face to face, and begin a scorpion waltz. In the laboratory, scorpion pairs have waltzed for two days. But in nature half an hour or so seems to suffice, with the dance terminating when the male locates a really choice piece of ground (the long laboratory waltz may occur because the male cannot find the right type of ground). Soil texture is important in scorpion sex because instead of a penis males have a detachable spike which must be firmly implanted in the ground if insemination is to occur. Once the spike is in place the male maneuvers his partner so that her genitals are atop it. As the spike bends under her weight two tiny valves open, through which the sperm is released.

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It’s difficult for human beings to see scorpions at night, but it’s easy for scorpions to see other scorpions. That is because scorpions produce bright green fluorescent light, which is clearly visible to them but invisible to the human eye. These superb adaptations have been honed by 400 million years of evolutionary experience during which countless billions of individual scorpions with blind spots, less sensitive pectines, or poor fluorescence have been weeded out, until finally we are left with the seemingly perfect, yet utterly alien, creatures here described.

If you imagine that worms are any less intriguing than scorpions, Attenborough has surprises for you. The largest worms on earth inhabit an area of about eleven square miles in Gippsland in southern Australia. It’s difficult to establish just how long these creatures are, for they keep changing shape from (relatively) short and squat to long spaghetti-like strands. Attenborough settles on a meter; but their changing shapes are hardly their most surprising attribute, for the giant Gippsland earthworm is more often heard than seen. As these subterranean creatures move about in their tunnels they produce sounds like water going down a plughole, or more occasionally like a toilet being flushed. The town of Poowong in West Gippsland supposedly derives its name from an aboriginal word describing the sound of the worms as they shift about: Pwwwong!

Every year or so the giant Gippsland earthworm deposits a case holding a fertilized egg in the wall of its burrow. It’s about the shape and size of a cocktail sausage, and if you hold it up to the light, inside you will see a single baby worm. By the time it hatches twelve months later it will already be eight inches long—larger than a normal earthworm. Such slow reproduction indicates that the worms are long-lived. They may be as old as you or I.

Biologists were recently asked to relocate a colony of giant Gippsland earthworms that lay in the path of a new highway. Each worm had to be painstakingly excavated and released into a new burrow. To their surprise the researchers discovered that the worms had different personalities: some were placid, others agitated at the intrusion; one was actually described as “aggressive.”* No one seems to know why.

Attenborough raises an analogous question of insect personalities when he discusses the bolas spider:

When we were filming…we had in front of us a line of bottles, each of which supported a spray of leafy twigs in which crouched a small bolas spider. These tiny creatures catch moths by whirling a filament of silk with a sticky blob at the end, whenever one came near them. Kevin Fleay, the cameraman, had been working with them for nearly a week and he introduced them to me individually. This one, he told me, was very shy. The slightest vibration made her draw up her legs and stay motionless no matter how near a moth came. That one reacted in the same way if the light was too bright. A third didn’t seem to mind how much light was shone on her but on the other hand she was unpredictable. Sometimes she would hunt and sometimes not. But the one at the end of the line, no matter how much she had eaten, or how much light shone on her, would whirl her bolas whenever a moth came anywhere near and usually caught her prey. These tiny creatures half the size of my fingernail each had individual characters.

The fact that invertebrates have characters seemingly similar in their fundamentals to those possessed by ourselves is a theme to which Attenborough returns repeatedly, and as he does so the gulf between the least and greatest of living things diminishes. But Life in the Undergrowth offers another revelation that seems to close that gap further. At a time when our rat-sized ancestors were still cowering in the shadows of the dinosaurs it is probable that certain insects had already created cities, farms, and skyscrapers, and today their descendants have become highly sophisticated indeed.

Among the most thought-provoking of such creatures are the ranchers. These ants carefully tend herds of sap-sucking aphids, tiny pear-shaped insects, which they milk for a sugary substance that makes good ant food. Just like human farmers, the ants ensure that their herds get the best possible forage. They do this by driving their aphids to parts of the plant that are rich in sap, and when the aphids produce young (which are miniature versions of the adults), the ants carry them to fresh pastures. Ant shepherds drive off aphid predators such as ladybirds, and in bad weather build shelters of leaf particles and soil to protect their livestock. They have even been observed marking their herds with a substance specific to one ant colony; it resembles our branding of livestock, Attenborough says. But most astonishingly, the ants have discovered how to interfere with the reproduction of their herds so as to maximize production; just as we castrate calves, so the ants feed their aphids a fluid which prevents them from reaching sexual maturity.

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Other ants and some termites have become farmers. They create great underground factory-farms of enormous complexity, within which they maintain conditions that promote the growth of nutritious fungi. The Bible commands us to look to the ant, but few would think to find there industries of such complexity and sophistication. The greatest of Earth’s architects and builders are the termites. These distant relatives of the cockroach build cities whose spires tower far higher above their inhabitants’ heads, relative to their size, than do our tallest skyscrapers. Some species in northern Australia build razor-backed structures that point north, maximizing the thermal comfort of those within. And in many species of termites the water provisioning, highway construction, and air conditioning of their great edifices rival in sophistication anything built by humanity.

With its superb synthesis of the majority of living species, Life in the Undergrowth is a high point in David Attenborough’s career, but it is also an elegant restatement of something he has spent a lifetime trying to teach: we are simply one species among a multitude, all of which are worthy of our interest and respect.

2.

Piotr Naskrecki has traveled the world with his camera, seeking out rare and little-known creatures, and The Smaller Majority is a book filled with some of the most beautiful wildlife photographs I have ever seen. He does not restrict himself to terrestrial invertebrates, but includes some smaller vertebrates such as lizards and amphibians. Some of his most dramatic photographs are of caecilians, which look like giant earthworms but are actually related to frogs and salamanders. A double-page spread is devoted to anatomical close-ups, revealing that caecilians have a tentacle where you might think the eye should be, while their anus is at the end of the body, which demonstrates that although caecilians are extraordinarily long and slender, they have no tail.

Naskrecki’s own specialty is the study of grasshoppers, to which he devotes a dozen or so pages. Some particularly vivid species are found in Australia, as is a locust troublesome to farmers, and Naskrecki has spent considerable time in the Australian outback documenting these creatures. He writes:

During a recent locust outbreak in Australia, the government launched a campaign aiming to introduce these insects into local cuisines. To help break the popular reluctance to eat locusts the Australian media started to refer to them as “sky prawns.”

The idea of Australians eating their way clear of a locust plague, or even tossing a “sky prawn” on the barbecue, seems remarkable to an Australian such as myself. Like their American counterparts, Australian bushmen love telling tall stories, and I suspect that the locust-obsessed visitor was judged fair game. In fact “sky prawns” are yet to be seen in the restaurants of Sydney and Adelaide, or even the outback.

In my search for the origins of the “sky prawn” story I turned to Jeffrey Lockwood’s excellent book Locust, where I discovered that people of many cultures relish the insects. Among the greatest consumers were the Goshute Indians of western Utah. One anthropologist estimated that a Goshute could harvest two hundred pounds of sun-dried grasshoppers in an hour—which would yield the equivalent calories of five hundred large pizzas. In a striking inversion of the “sky prawn” story, the Goshute, when they were first given prawns to eat, called them “sea crickets.”

The sea cricket is a mere diversion in Lockwood’s book, whose central theme is the tale of the American locust and its impact upon the shaping of the West. As the American frontier rolled westward, a continent of superlatives was revealed to the world: trees taller, older, and grander than any seen before; billion-strong flocks of passenger pigeons whose droppings whitened the ground like snow; and buffalo herds that took days to pass and whose lowing was heard hours before the creatures came into view. Although some of those wonders are now just memories, they still help define the frontier. Yet the most abundant creature that ever roamed the West is not even a memory. The Rocky Mountain locust is both gone and forgotten. Its disappearance is, according to Lockwood, “the quintessential ecological mystery of the North American continent—a century-old homicide on a continental scale.”

Locusts are simply grasshoppers with peculiar habits. There are ten species worldwide, and they are characterized by their roving swarms, which can appear out of nowhere and can devastate crops over a considerable area. Each continent has its own locusts, and each species has evolved independently from less troublesome grasshopper relatives. The Rocky Mountain locust—the sole species recorded from North America—was the most numerous and devastating of them all. Some idea of its abundance can be gained from the size of a swarm that visited Nebraska in 1875. Known as Albert’s Swarm (named for the Weather Service pioneer who documented it), it is estimated to have consisted of 3.5 trillion insects. That’s six hundred for every person living on earth today.

Some sense of what that visitation was like was conveyed by Laura Ingalls Wilder in On the Banks of Plum Creek from the Little House on the Prairie series. Before the swarm arrived, she sensed that

the light was queer. It was not like the changed light before a storm. The air did not press down as it did before a storm. Laura was frightened, she did not know why….

A cloud was over the sun. It was not like any cloud they had ever seen before. It was a cloud of something like snowflakes, but they were larger than snowflakes, and thin and glittering. Light shone through each flickering particle….

The cloud was hailing grasshoppers. The cloud was grasshoppers. Their bodies hid the sun and made darkness.

The next morning Laura found that the prairie grass had been mowed down and the trees stripped of their fruit and leaves. In fact locusts seem to have eaten almost anything, from green paint to window blinds and dead bats and live birds—even other locusts. A favorite food was the wooden handles of tools that had absorbed the salty sweat of the pioneers. Such habits induced a loathing in the homesteaders; and of course in the wake of the swarms came starvation.

Throughout the 1870s, military posts across the American frontier dispatched reports on the devastation left by the locust swarms. Each tells only a local story, but when they are put together the extent of the destruction becomes clear. One poignant account from Missouri’s St. Clair County reads

We have seen within the past week families which had not a meal of victuals in their house…. In one case a family of six died within six days of each other from the want of food to keep body and soul together…. From present indications, the future four months will make many graves, marked with a simple piece of wood with the inscription “Starved to death,” painted on it.

Because locust plagues loom large in the Old Testament as a form of divine retribution, some settlers were discomfited morally as well as physically by the swarms. But others saw in them an opportunity to boost their religious convictions. Around the Great Salt Lake, the pickled bodies of locusts that had drowned piled six feet high along the shoreline. According to the Mormon farmer and railroad grader Milando Pratt, the rotting bodies put forth a “great stench…and cast the aroma of this slowly melting putrid wall upon the windward breezes to be wafted earthward toward our suffering camp.” Starving and beset by stinks, the Mormon settlers must have been tempted to read the plague as a divine order to move on. Their leaders, however, took a different view, for the locust visitation fitted in with their interpretation of the Sabbath.

According to Mormon theologians there are varying Sabbath cycles: a Sabbath one day in seven, and a Sabbath year, known as a jubilee, one year in seven. During the jubilee year the earth should be allowed to rest, with no farming to take place; instead the observant should subsist from a surplus garnered and stored during the preceding six years. Lockwood writes:

As bad luck or divine providence would have it, the locusts began to arrive the year that the Mormon farmers failed to observe a Sabbath, and the insects bred prolifically and continued their devastations into the following year.

A prominent church official, Heber C. Kimball, put matters succinctly:

How many times have you been told to store up your wheat against the hard times that are coming upon the nations of the earth?… It only requires a few grasshoppers to make the earth rest, they can soon clear it. This is the seventh year, did you ever think of it?

Respite came from an unexpected quarter. The flag of Salt Lake City bears a seagull. It may seem odd that this predominantly coastal bird should figure as an emblem of an inland city, but seagulls reputedly arrived en masse in the wake of the locusts and thinned their ranks considerably.

With seagulls in short supply over the rest of the West, other pioneers resorted to desperate methods, including horse-drawn flamethrowers, gigantic locust-crushers, and coal-tar- coated hopper-dozers, but all proved useless. Then, in the closing decades of the nineteenth century, the locust swarms stopped coming—and, astonishingly, hardly anybody noticed. This was partly because other kinds of grasshoppers became abundant around the same time, and partly because people kept expecting another big plague. The last time anybody saw a Rocky Mountain locust alive was in 1902, and it was only years later that it began to dawn on people that there would never be another swarm—because the most abundant insect ever recorded was extinct.

Just ten years after that final sighting, an entomologist working in Russia made a remarkable discovery that threw just about everything entomologists thought they knew about locusts into disarray. Boris Petrovich Uvarov was studying locust outbreaks around the Caspian Sea when he saw something he thought inexplicable—a grasshopper transformed itself into a locust. It was, a colleague wrote, as if he was seeing evolution unfolding before his eyes. Yet what he had discovered was not evolutionary change but something very different, which came to be known as the theory of phases.

The grasshopper, Locusta danica, is a bright green, solitary creature that causes no harm to farmers. If their density increases, however, the next generation becomes black and red, long-winged, and prone to travel long distances. Uvarov discovered that the smell of grasshopper feces and the frequent disturbance of the tiny hairs on the grasshopper’s hind legs caused by crowding together with other grasshoppers were the key cues leading to transformation. And he discovered that the changes were entirely reversible: when the numbers dropped, the next generation would develop into solitary, green grasshoppers.

This remarkable discovery opened the possibility that the Rocky Mountain locust may not be extinct after all: perhaps it, too, had phases, and its solitary phase was still lurking somewhere in the West, awaiting the conditions needed to spark its transformation. The theory had many powerful adherents, and some American entomologists even claimed that they had, in the laboratory, forced grasshoppers to transform themselves into Rocky Mountain locusts. Then, in the late 1950s, a study of male genitalia provided a definitive answer to the riddle. Grasshopper phalluses are precise tools: each species has its own shape, and each will fit only into a female of the same species. Study of the seventeen Rocky Mountain locusts preserved in museum collections revealed that their phalluses were unique. Thus they were not a phase of another species.

While many might read a moral tale in the locust’s extinction—perhaps that it’s unwise to mess with the Mormons—entomologists took a more objective view. Some thought that the spread of alfalfa, which disagreed with the creature’s digestion, might be the cause; others felt that the demise of the buffalo was somehow involved. Jeffrey Lockwood, however, had his own ideas. He figured that the outbreaks had to come from somewhere and that if the cradle of the swarm could be identified, then so would the cause of the creature’s extinction. The swarms, he established, originated in the high valleys of the Rocky Mountains. The species probably required just three thousand square miles as its nursery, and may actually have used far less. At around the time the locust vanished, the high valleys were being settled. Grazing, irrigating, and cropping, it seems, transformed the vital nurseries in ways that made them inhospitable to locusts. Thus a few farmers banished from the land a creature that once rivaled or even exceeded the passenger pigeon in abundance, and which had threatened farming across a vast region.

At the very end of his fascinating book Lockwood takes us to Yellowstone National Park, whose fertile valleys were set aside as a reserve in 1872. The park had acted as a last refuge for the buffalo, and Lockwood wondered whether the locust might have survived there also. He writes that among the first grasshoppers he collected there was a female with spectacularly long wings. Of course the females of locust species are very difficult to identify, for they lack phalluses. More recently he captured several similar individuals. “I think I know who they were,” he confides, “so I released them back into the field. Because I did not remove them from the park, their identities and location need not be reported to the authorities.” Perhaps echoes of the frontier will once again be seen in America.

This Issue

March 23, 2006