On Trails

by Robert Moor

  As a species, humans straddle a line between external and internal intelligence. With big brains and (typically) small clan size, humans have traditionally harnessed individual cleverness to outcompete rivals for food and mates, to hunt and dominate other species, and, eventually, to seize control of the planet. As later chapters will show, we have also externalized our wisdom in the form of trails, oral storytelling, written texts, art, maps, and much more recently, electronic data. Nevertheless, even in the Internet era, we still romanticize the lone genius. Most of us—especially us Americans—like to consider any brilliance we may possess, and the accomplishments that have sprung from it, as being solely our own. In our egotism, we have long remained blind to the communal infrastructure that undergirds our own eureka moments. This egotism extends to our regard for pathways: when we write about trails, we tend to describe them as the creation of a single “trailblazer,” whether it is Daniel Boone blazing the Wilderness Road or Benton MacKaye dreaming up the Appalachian Trail. The reality of how most trails form—collectively, organically, without the need of a designer or a despot—has been increasingly apparent to scientists for centuries, but has remained invisible to most of us for far too long.

 

  The story of how we grew wise to the wisdom of insect trails begins, oddly enough, with the lowly caterpillar. One spring day in 1738 a young Genevan philosophy student named Charles Bonnet, while walking through the countryside near his family’s home in Thônex, found a small, white, silken nest strung up in the branches of a hawthorn tree. Inside the nest were squirms of newly hatched tent caterpillars, which bristled with fiery red hairs.

  At just eighteen years old, frail, asthmatic, myopic, and hard of hearing, Bonnet was a somewhat unlikely naturalist. But he was blessed with patience, attentiveness, and a relentless, burning curiosity. As he approached the cusp of adulthood, his father had begun pressuring him to become a lawyer, but he wanted to spend his life exploring the microcosmos of insects and other tiny creatures, a profession that had scarcely yet been invented.

  Bonnet decided to cut down the hawthorn branch and carry it back home. At the time, most naturalists would have sealed the caterpillars in a powder jar, called a poudrier, to better inspect their anatomy. But Bonnet wanted to observe the caterpillars’ natural behavior wholly unobstructed, en plein air, yet from the comfort of his home. He struck upon the idea of mounting the hawthorn branch outside the window frame of his study. That window soon became a kind of antique television, a glass screen displaying a miniaturized world, before which he spent countless rapt hours.

  After two days of patiently waiting for signs of life, Bonnet watched the caterpillars emerge from their nest and begin to march in single file up the windowpane. After four hours, the procession had successfully scaled the window; then it turned around. In descending, strangely, the caterpillars followed the exact path they had climbed. Bonnet later wrote that he even traced their route—presumably, with a wax pencil on the windowpane—to see if they ever deviated from it. “But they always followed it, faithfully,” he wrote.

  Each day Bonnet watched as the caterpillars mounted exploratory expeditions across the windowpane. Paying closer attention, he noticed that as they crawled, each caterpillar laid down an ultra-fine white thread, which the others followed. Curious, Bonnet rubbed his finger across their trail, breaking the thread. When the leader of the returning party arrived at the rupture, it turned back, apparently confused. The one behind it did the same, and the one behind that. Each subsequent caterpillar plodded calmly along until it reached the gap in the trail, at which point it either turned around or stopped to feel about for the thread, like a man groping for a dropped flashlight. Finally, one of the caterpillars, which Bonnet deemed “hardier than the others,” dared to venture forward: a thread was extended across the void, and the others followed.

  Emboldened, Bonnet collected more caterpillar nests, which he placed on his mantel. Soon, scores of caterpillars were exploring his bedroom, meandering across the walls, the floor, even the furniture. Feeling, no doubt, like a small new god, Bonnet found he could control where the caterpillars traveled simply by erasing certain trails. He delighted in showing this trick to visitors. “You see these little caterpillars who walk in such good order?” he would ask. “Well, I bet you that they will not pass beyond this mark”—and he would swipe his finger across their route, stopping them cold.

 

  Along the southern stretches of the Appalachian Trail, I too sometimes encountered mysterious little white tents in the crotches of trees. Occasionally they grew to monstrous proportions; I would turn a corner to find a tree wholly enveloped in a polygonal cloud. “Mummy trees,” my fellow hikers called them.

  For a reason I couldn’t quite place, they gave me the shivers. Tent caterpillars, I would later learn, are essentially creepy animals. Their faces resemble black masks, and their bodies are quilled over in fine, toxin-tipped spines, which can detach and float for more than a mile on a windy day, causing rashes, coughing fits, and pink eye. Some species of tent caterpillar undergo rampant population booms on a ten-year cycle, covering the countryside like spilled oil. In June 1913 a stream of forest tent caterpillars climbed up onto the tracks of the Long Island Rail Road; the rails were soon so thickly slathered with their remains that the wheels of approaching trains spun in place.

  A biologist named Emma Despland once told me about the time she walked into a stand of sugar maples during a tent caterpillar outbreak. She described it as a “ghost forest.”

  “It’s June and there are no leaves on the trees, and there are these big strands of gunky silk, like Halloween decorations,” she said. “And then you hear this rain falling. Except it’s not rain. It’s caterpillar poop.”

  Even among biologists, tent caterpillars are little loved. And yet for centuries, researchers like Despland have been studying them for one reason in particular: as consummate followers—perfectly faithful, perfectly foolish—tent caterpillars represent a reductio ad absurdum of what it means to follow a path. Despland told me that if you were to remove a younger caterpillar from its nest mates, it would spend all its time waving its head around in confusion, looking for a trail, and probably starve to death. Alone, they are utterly hopeless, and yet collectively they can denude entire forests.

  Curious to see firsthand how such timorous creatures manage to bind together and thrive in the world, I took the bus to Montreal to visit Despland’s lab, where she studies the forest tent caterpillar. When I arrived she peeled open a Tupperware container to show me the caterpillars: a smattering of fuzzy black critters, like mouse turds come to life. Then, on an old desktop computer in her office, Despland showed me time-lapse video of an experiment she had been conducting to determine how they find food. In the experiment, the caterpillars were placed in the middle of a cardboard runway. On the extreme left end of the cardboard strip was a Quaking Aspen leaf, which caterpillars especially love to eat. On the right was the leaf of a hybrid poplar, Populus trichocarpa × P. deltoides (clone H11-11), which they find unappetizing. The experiment was simple: It was as if a group of blindfolded children were placed in the middle of a long hallway, which held a piece of chocolate cake at one end and a pile of raw celery at the other. Asked to find and share the more delicious item, children could quickly solve the problem by splitting up and calling out to one another. But how would the caterpillars?

  Displayed on Despland’s computer monitor were five strips of cardboard, on which five experiments were being conducted simultaneously, but she directed my attention to the second from the bottom, where, over the course of many minutes, a group of caterpillars had mistakenly ventured over to the hybrid poplar leaf. Others followed their trails, and soon the whole nest was crawling on the broad green leaf, though they ate virtually none of it. For an uncomfortably long period of time they failed to correct this initial mistake. They followed their trail back to their “bivouac” (a silken pad, w
hich they construct as a resting place) in the middle of the strip, and then back to the hybrid leaf on the right, but none ventured to the left, where the tasty aspen leaf lay. It seemed each caterpillar would continue to follow the others to the hybrid leaf, leaving more trails, and more feedback, forever.

  I recalled a peculiar incident Bonnet had once described witnessing, in which a group of pine processionary caterpillars mistakenly formed a circular trail leading all the way around the rim of a ceramic vase. The details are scant, but it seems they continued marching around and around for at least a whole day. This same phenomenon was later famously observed by Jean-Henri Fabre: to his amazement, the caterpillars walked in circles for more than a week before they finally broke the ouroborosian loop and escaped. In Pilgrim at Tinker Creek, Annie Dillard recounts the horror she felt while reading Fabre’s portrait of these soulless, circling automatons. “It is the fixed that horrifies us,” she wrote. “It is motion without direction, force without power, the aimless procession of caterpillars round the rim of a vase, and I hate it because at any moment I myself might step to that charmed and glistening thread.”

  Despland’s caterpillars seemed to be caught in a similarly brainless loop. For more than an hour, the pattern continued: the caterpillars returned to their bivouac, returned to the hybrid leaf, and returned to the bivouac again. I began to squirm.

  Eventually, a small contingent broke away and ventured off in the opposite direction. They traveled slowly, with excruciating hesitancy, inching, ducking, cowering, stalling, nudging one another forward, and frequently turning back. Despland guessed that their hesitancy springs from a genetic aversion to ending up away from the pack, alone, where they could get picked off by a bird.

  By the end of the second hour, the scouting party had finally made it to the aspen leaf, and others subsequently followed the trail they had blazed. Despite their initial misstep, by hour four all the caterpillars had found the correct leaf and gnawed it to a husk.

  The foraging technique of these caterpillars is remarkably simple, even idiotic, but it works. The fail-safe, Despland explained, is that hunger induces restlessness, which eventually compels them to abandon the well-worn trails and go looking for something else. “The leaders tend to be the hungry ones,” she explained. “Because they’re the ones who are willing to pay the cost.”

 

  One year after his initial caterpillar experiments, Charles Bonnet was outside hunting for a new batch of caterpillars when he happened across a prickly flower called a teasel, whose head harbored a colony of tiny red ants. Ever curious, he plucked the flower, carried it back to his study, and planted it upright in an open powder jar.

  One day Bonnet returned to discover that a number of the ants had deserted the nest. Searching about, he found them marching up his wall to nibble the wood at the top of his window frame. In his journal, Bonnet described watching one ant as it climbed down the wall, up the side of the powder jar, and back to the nest. At the same time, two ants emerged from the teasel head and climbed to the top of the window frame, following precisely the same route that the other had just descended.

  “Instantly, it came to my mind that these ants which I had in front of me, like the caterpillars, left a trace that directed them in their course,” he recalled.

  Of course, he knew that ants did not emit a thread. But they did give off a strong smell, which is sometimes described as being reminiscent of urine. (This odor lent ants their archaic name, “pismires,” and later, “piss-ants.”) The substance, Bonnet theorized, could “more or less adhere to objects they touch, and then act on their sense of smell.” He compared those “invisible traces” with the trails of wildcats, which are imperceptible to humans but plain as blood to dogs.

  His suspicion was easily tested: as before, he rubbed his finger across the ants’ pathway. “Doing so, I broke the path on a width equal to that of my finger, and I saw precisely the same spectacle the caterpillars had given me: the ants were diverted, their walk was interrupted, and their confusion amused me for me some time.”

  Bonnet had stumbled on an elegant explanation for how ant trails form, which required neither powerful memories, strong eyesight, nor simple language (as Huber and Fabre later proposed). Bonnet theorized, correctly, that ants ordinarily follow trails that lead to their homes and to food sources. However, some ants wander off track, “attracted by certain smells or other sensations to us unknown,” spawning new side roads. If that rogue ant finds food, it will leave a new trail on its return to the nest, and other ants will follow. So, wrote Bonnet, “a single ant can lead a large number of its companions to a certain place without any need of a particular language whereby it announces the discovery that it has just made.”

  Judging from his journals, Bonnet seems not to have realized how historic this discovery was. Scientists had long suspected that ants deposit chemicals when they walk; in the sixteenth century, two German botanists, Otto Brunfels and Hieronymus Bock, discovered that ants produce formic acid after noticing that a blue chicory flower, when thrown onto an anthill, turns a vivid red. But no one properly connected the dots until Bonnet.

  Around the time of Bonnet’s death in 1793, the zoologist Pierre André Latreille confirmed Bonnet’s suspicion that ants sniff their way through the world. He learned this by amputating the antennae from a number of ants; at once, he wrote, they began wandering aimlessly about, as if in “a state of intoxication or a kind of madness.” Then, in 1891, Sir John Lubbock, the English polymath, performed a groundbreaking series of experiments involving Y-shaped mazes, bridges, and rotating platforms. Through painstaking experimentation, he showed that Lasius niger ants navigate primarily by using scent trails.

  In the late 1950s, E. O. Wilson solved the riddle by locating the gland in fire ants that secretes trail pheromones. He had a hunch that the trail substance resided somewhere in an ant’s abdomen, so he split the abdomen open and, using a pair of sharpened watchmaker’s forceps, carefully removed all the organs. Then he smeared each organ across a piece of glass. After each stroke, he checked to see if it had any effect on a nearby colony of ants. Line after line, organ after organ—the poison gland, the hindgut, the little blob of lipids called a “fat body”—prompted no response. Finally he smeared out a tiny, finger-shaped organ called Dufour’s gland. “The response of the ants was explosive,” Wilson later recalled. “As they ran along they swept their antennae from side to side, sampling the molecules evaporating and diffusing through the air. At the end of the trail they milled about in confusion, searching for the reward not there.”

  By the year 1960, our fuzzy understanding of ant trails had snapped into sharp focus. Two crucial new terms were born concurrently: a pair of German biologists coined the term pheromone—chemical triggers, or signals—and Pierre-Paul Grassé introduced the notion of “stigmergy.” Stigmergy is a form of indirect communication and leaderless cooperation, using signals deposited in the environment. Termites, for example, organize their massive construction efforts stigmergically: there is no foreman, and no direct communication between the termites. Rather, the termites respond to a series of simple cues in the environment (if dirt here, move dirt there), which in turn impel them to further alter the environment. This behavioral feedback loop can result in structures of stunning efficiency and resilience, like the towering termite mounds of Australia, which, proportional to their makers, are three times taller than our highest skyscrapers. With a combination of pheromones and stigmergy, even the simplest insects could build labyrinthine trail systems.

  In the 1970s a biologist named Terrence D. Fitzgerald, being familiar with Wilson’s work, intuited that tent caterpillars might also use trail pheromones. At the time, biologists believed that tent caterpillars followed their nest mates’ silk, which is expelled from their mouthparts, but he had a hunch that they were secreting trail pheromones onto the silk from their back ends, as ants do. So he folded a plain piece of paper in hal
f and ran its edge along the underside of a caterpillar’s abdomen. Then he unfolded the paper and placed some caterpillars on it. Sure enough, the caterpillars marched back and forth along that crease, following the invisible line of pheromones just as Wilson’s fire ants had. (Like Wilson, Fitzgerald was later able to isolate and synthesize these trail pheromones.) This discovery lent a neat symmetry to the path of inquiry Bonnet had started: We learned ants follow pheromone trails by studying tent caterpillars, then we learned tent caterpillars deposit pheromone trails by dissecting ants.

  It may seem odd, then, that neither Wilson nor Fitzgerald cites Bonnet’s discovery. In fact, many of Bonnet’s writings, including the story of how he discovered the true nature of ant trails, have never been published in English. Though his career showed a promising start, it ultimately veered off on an ill-fated path. In his twenties, Bonnet became a celebrated naturalist: the first person to witness a virgin birth among plant lice, the first to describe regeneration among worms, the first to learn that caterpillars breathe through holes in their skin, and the first to prove that leaves exhale. Then, in a cruel twist, his vision began to cloud with cataracts. Unable to practice observational science, he turned to more cerebral fields, like philosophy, psychology, metaphysics, and theology. Much of the latter half of his life was spent trying to reconcile the confusing new findings of the biological sciences with his deep religious faith, which held that the world was divinely engineered. Bonnet’s magnum opus—an all-encompassing theory of the universe called the “Great Chain of Being,” which posited that all species were slowly progressing toward a state of perfection over the course of eons—had some influence on later evolutionary theorists like Jean-Baptiste Lamarck and Georges Cuvier. But in the broader span of scientific progress, it proved little more than a theoretical side road, which was later made obsolete by Darwin’s theory of evolution by natural selection. By the end of his life, Bonnet’s blindness caused him to suffer from phantasmagoric visual hallucinations, which are now known as Charles Bonnet syndrome.I Today, that syndrome is primarily what he is remembered for, when he is remembered at all.