The Trailhead Queen was dead. At first, there was no overt sign that her long life was ending: no fever, no spasms, no farewells. She simply sat on the floor of the royal chamber and died. As in life, her body was prone and immobile, her legs and antennae relaxed. Her stillness alone failed to give warning to her daughters that a catastrophe had occurred for all of them. She lay there, in fact, as though nothing had happened. She had become a perfect statue of herself. While humans and other vertebrates have an internal skeleton surrounded by soft tissue that quickly rots away, ants are encased in an external skeleton; their soft tissues shrivel into dry threads and lumps, but their exoskeletons remain, a knight’s armor fully intact long after the knight is gone. Hence the workers were at first unaware of their mother’s death. Her quietude said nothing, and the odors of her life, still rising from her, signalled, I remain among you. She smelled alive.

The deception was made easier by the fact that in life she had never given orders or led them in activities of any kind—even though she could have performed all their tasks if she chose. She had taken the only initiatives she ever took all in a burst, at the beginning of her adult life, when she had abandoned the colony of her birth and, along with it, her mother and her sisters. First, she had spread her four membranous wings and flown into the air. There, she’d joined a swarm of flying males and other virgin queens. One of the males had caught her. He’d clamped his legs around her body, and the couple had spiralled down to the ground. On landing, he had used the large claspers at the rear end of his body to hold their genitalia together as he completed the insemination. Within five minutes, the act was finished, and the queen shook the male loose. All the sperm she had received flowed up into a special bag-shaped organ in her abdomen, where it would stay until called on to fertilize her eggs. It might last for years into the future. Each sperm was endowed with a potential life span equal to her own.

In contrast, the father of all her children was programmed to die almost immediately after the mating. The only thing that he had ever done was accept meals regurgitated to him by his sisters, as if he were a nestling bird, and wait, and wait some more, and finally take the one short flight from his home, followed by five minutes of copulation. In other words, the male was no more than a guided missile loaded with sperm, his life’s work a single ejaculation. Afterward, he was left with only one instruction, to be enforced if necessary by his sisters: Don’t come back. He had been issued a one-way ticket. He had no chance at all of survival. A delicate creature, he could not find food, or feed himself if he stumbled across some. He would die by dehydration, or crushed in the beak of a bird, or chopped into pieces by the jaws of an enemy ant, or, less quickly, pierced by the bloodsucking proboscis of an assassin bug.

To escape the same fate, the newly mated future Queen of the Trailhead Colony, full-brained and powerfully muscled, hurried to find shelter. She had to get back underground as quickly as possible. First, however, she had to take a few minutes to shed her wings. To do that, she simply bent her middle legs forward, pressed them against the base of the wings, and snapped them off. This mutilation caused no injury to the rest of her body; it caused no pain. The Queen was a parachutist who slipped her harness upon landing. Now she could move more quickly to avoid the ants, spiders, and other predators hunting around her in the grassroots jungle.

Soon she came upon an open space between grass clumps, a small clearing at the Lake Nokobee trailhead. By luck she had found an ideal site to build a nest. She began at once to dig a vertical tunnel in the sandy clay soil. Her movements were swift and precise, and within minutes she had deepened the shaft to more than her body length. This provided her some degree of protection, but she needed to proceed as quickly as possible. Her life remained in constant danger.

At a predetermined depth, which she measured by the time it took her to climb up and down the shaft, the young Queen turned to the side and began to excavate a wider space. She continued until she had fashioned a round chamber about three times wider than the vertical shaft. Her safety was now enhanced but not insured. Predators and marauding ants could still climb down the shaft to attack her. But at least now the enemies would be confined to a narrow space by the walls of the shaft and forced to confront the young Queen’s thrusting stinger and snapping jaws head on before they could reach her vulnerable body.

Even with the excavation of the first chamber complete, the Trailhead Queen had heavy work ahead. First, she laid a small cluster of eggs on the earthen floor. These tiny objects she was compelled to lick continuously. It was an urgent task: to the peril from enemies above was now added the threat of bacteria and fungi teeming in the soil all around her. If the eggs were not regularly cleaned and coated with antibiotic saliva, they would soon be overgrown by an invading mold and consumed. From a single bacterium in the soil, millions could proliferate on any ant tissue left unprotected.

But the dice fell right for the Queen of the Trailhead Colony. As tiny larvae hatched from her eggs, she fed them food secreted from a large gland that partly filled her head and emptied through her mouth. This baby food was manufactured from her own fat stores and was created by the metabolism of her now useless wing muscles. From the reserves of her own body, the young Queen reared a dozen workers. All were female. They were tiny and weak, barely able to perform the work necessary for the little colony to survive. By necessity, they came into the world as midgets. If each had been larger, fewer of them could have been reared—too few to provide sufficient labor for the survival of the newborn colony.

Some of these pioneers, guided entirely by instinct, because no one existed to teach them, set out to forage for food. Others took care of the Queen and reared the next generation of workers to maturity. Still others devoted time to enlarging the nest. Failure to perform all these tasks with exactitude would have meant death for the colony. The young Queen could no longer help. She herself desperately needed help to continue living. Her expendable body tissues were depleted. They had almost all been fed to the larval daughters, and now she was starving.

The first foragers venturing timidly away from the nest were able to bring back a few scraps of food. Their prizes included a fallen mosquito, a bit of shed caterpillar skin, and a newly hatched spiderling, which was enough to keep the colony alive and allow the Queen to regain some of her weight and strength. The workers of the next generation, raised on food harvested from terrain outside the nest, were somewhat larger and stronger than the first generation. They began to dig out more tunnels to accommodate the growing population. As the colony expanded, its home became a labyrinth of chambers and connecting galleries—an enemy-proof fortress. A mound of excavated soil formed above it, reinforcing the roof and retaining the warmth of the sun.

As the months passed, the Queen, growing heavy with egg-filled ovaries, retreated ever deeper into the earth, distancing herself from the still dangerous nest exterior. She had become an extreme specialist: she laid eggs, while the workers performed all the labor necessary to raise her offspring, their sisters. They were the Queen’s hands and feet and jaws, and increasingly they replaced her brain. They functioned together as a well-organized whole, dividing up the tasks without regard to their own welfare. The Trailhead Colony began to resemble a large, diffuse organism. In a word, it became a superorganism.

By the time the colony had reached its full mature size, two years after the nuptial flight of the Queen, it contained more than ten thousand workers. It was able, in the following year, to rear virgin queens, and males, and through them to give birth to new colonies. By that time the Queen was producing eggs at the average rate of one every fifteen minutes. Heavy and torpid, she lay in the royal chamber at the bottom of the subterranean nest, five feet below the surface, a distance of four hundred ant lengths. By human scale, the ant city was the equivalent of two hundred underground stories. The mound of excavated soil capping the nest added another fifty stories aboveground.

The Queen may not have been the leader of this miniature civilization, but she was the fountainhead of all its energies and growth, the key to its success or failure. The metronomic pumping out of fertilized eggs from her twenty ovaries was the heartbeat of the colony. The ultimate purpose of all the workers’ labor—their careful construction of the nest, their readiness to risk their lives in daily searches for food, their suicidal defense of the nest entrance—was that she continue to create more altruistic workers like themselves. One worker, or a thousand workers, could die and the colony would go on, repairing itself as needed. But the failure of the Queen would be fatal.

Now, after twenty more years, the catastrophe had occurred. The death of the Queen was the greatest challenge the colony had faced since the days of its founding. Yet the workers could not take action until they were certain that the Queen was dead. Already, they knew that something was not right, that something unnamed had settled upon them, but they did not yet realize the extent of the problem. So the Trailhead Colony thrummed on for a while longer with bustle and precision. Like a large ship at sea, it could not be easily diverted from the shoals in front of it.

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Because ants live most of their lives in underground darkness, they cannot communicate through sight or sound. Pheromonal, they think only in taste and smell. The members of the Trailhead Colony transmitted their messages using about a dozen chemical signals, which they picked up by smelling one another constantly with sweeps of their antennae. An ant who was well fed said to a less well-fed nest mate, Smell this, and if you are hungry eat. If the ant approached and was in fact hungry, she extended her tongue, and the donor ant rewarded her by regurgitating liquid directly into her mouth. When a wood thrush flew by the Trailhead mound carrying a grasshopper to her own nest and dropped part of the crushed insect to the ground, a patrolling worker found it in less than a minute and triggered a chain action. The worker examined the grasshopper, tasted it briefly, then ran back to the nest entrance. On the way, she touched the tip of her abdomen repeatedly to the ground, laying down a thin trail of chemicals. Entering the nest, she rushed up to each nest mate she passed, brushing her face close to theirs. With their antennae, her nest mates detected both the trail substance and the smell of grasshopper. The signals now proclaimed, Food. I have found food. Follow my trail! Soon a mob of ants ran out, followed the trail, and gathered around the delicious grasshopper haunch. Some of the first to arrive ran back to the nest, laying trails of their own, reinforcing the message, saying, Come on, come on, we need help. The ants still by the grasshopper piece began to drag it toward the nest entrance. A catbird perched on the branch of a nearby tree saw the activity and swept down to investigate. She pecked at the grasshopper, scattering the ants and injuring several. The ants expelled a pheromone from a gland that opened at the base of their jaws. A chemical vapor spread fast. It shouted, Danger! Emergency! Run!