Naturalist 25th Anniversary Edition

by Edward O. Wilson

THEY ARE EVERYWHERE, DARK AND RUDDY SPECKS THAT zigzag across the ground and down holes, milligram-weight inhabitants of an alien civilization who hide their daily rounds from our eyes. For over 50 million years ants have been overwhelmingly dominant insects everywhere on the land outside the polar and alpine ice fields. By my estimate, between 1 and 10 million billion individuals are alive at any moment, all of them together weighing, to the nearest order of magnitude, as much as the totality of human beings. But a vital difference is concealed in this equivalence. While ants exist in just the right numbers for the rest of the living world, humans have become too numerous. If we were to vanish today, the land environment would return to the fertile balance that existed before the human population explosion. Only a dozen or so species, among which are the crab louse and a mite that lives in the oil glands of our foreheads, depend on us entirely. But if ants were to disappear, tens of thousands of other plant and animal species would perish also, simplifying and weakening land ecosystems almost everywhere.

  They are intertwined in our world, too, as illustrated by an incident that occurred in Harvard’s Biological Laboratories in the late 1960s. At the risk of melodrama I will call it the Revenge of the Ants. The serious trouble began when an assistant in Mark Ptashne’s laboratory, a humming center of research on gene repression, began the routine pipetting of sugar solution for the culture of bacteria. She could not draw the liquid through. Looking more closely, she saw that the narrow pipette channel was plugged with small yellow ants. Other, more subtle signs of a strange invasion had been noted in the building. Here and there yellow ants quickly covered food left out after lunch or afternoon tea. Portions of breeding colonies, with queens and immature stages surrounded by workers, appeared miraculously beneath glass vessels, in letter files, and between the pages of notebooks. But most alarming, researchers found the ants tracking faint traces of radioactive materials from culture dishes across the floors and walls. An inspection revealed that a giant unified colony was spreading in all directions through spaces in the walls of the large building.

  I had reason to be concerned with the invasion. It had started by accident in my own quarters. The species was Pharaoh’s ant, known to specialists by its formal name Monomorium pharaonis, a notorious pest of East Indian origin that infests buildings around the world. When a supercolony occupies hospitals, its workers feed on surgical waste and the wounds of immobilized patients, in the course of which they sometimes spread disease organisms. Portions of colonies transport themselves by moving into luggage, books, clothing, and any other objects with one or two inches of space. Arriving at a new accidental destination, which might equally well be an apartment house in Oslo, a florist shop in St. Louis, or a vacant lot in Caracas, they move out and commence to breed.

  Harvard’s propagule, as we reconstructed its history later, took passage in the airport at the Brazilian port city of Belém. Portions of a supercolony entered two wooden crates belonging to Robert Jeanne, a Ph.D. candidate studying under my direction. Now a professor of entomology at the University of Wisconsin, Jeanne in 1969 was homeward bound after a lengthy period of field research in the Amazon rain forest. By the time he opened the crates in the Biological Laboratories and discovered the hitchhikers, the ants had established themselves in the walls and were metastasizing.

  To eliminate a large population of Pharaoh’s ants by conventional means can be expensive and disruptive. An ingenious alternative solution was devised by Gary Alpert, a graduate student in entomology with a special interest in pest control. He was counseled and aided by Carroll Williams, Harvard’s professor of insect physiology. Williams provided a chemical compound that mimics the action of the juvenile hormone of insects by sterilizing queens and preventing the full development of the larvae into the adult stage. By mixing this compound with peanut butter, Alpert fashioned baits that he hoped the foraging ants would carry back into the nests and thus spread its stultifying effect. The method was then in its earliest experimental stage, but it worked. Over a period of months the ant population steadily declined. After two years, it disappeared.

  The saga of the Pharaoh’s ants was, however, not quite over; it was to end on the pages of science fiction. The incident inspired the plot of the 1983 novel Spirals, by William Patrick, then the editor for biology and medicine at Harvard University Press. His imaginary ants were suspected of carrying around the laboratory a form of engineered DNA that induced progeria, a disease that fatally accelerates the process of aging. The daughter of a key bioengineer died from the condition, turning into a physiological old lady before she got past her childhood years. In the end the ants were exonerated, when the researcher himself proved at fault: he had cloned the daughter from cells of his dead wife, and her development had gone awry as a result.

  One does not need to make ants protagonists of a novel to bring them deserved attention. I placed them at the center of my professional life, the focus of a near obsession, and I think I chose wisely. Yet I also confess that at the time their main appeal was not their environmental importance or the drama of their social evolution. It came from the discoveries they generously offered me. I built my career from easy revelation. The most important topic I addressed was their means of communication, which led me into a long period of productive research on animal behavior and organic chemistry.

  My interest in chemical communication began in the fall of 1953, when Niko Tinbergen and Konrad Lorenz visited Harvard University to lecture on the new science of ethology. Twenty years later they shared the Nobel Prize for physiology or medicine, with Karl von Frisch as a third corecipient, for the years of work chronicled during their American tour. Tinbergen, a precise, carefully spoken Dutchman, arrived first. He gave an account of ethology that struck me with the resonance of important discovery. Because I was absorbed in systematics and biogeography, however, subjects remote from behavior, I took only a few notes and otherwise paid little attention. Then Lorenz came. He recounted his work begun in the 1930s, which he now was continuing at the Max Planck Institute in Buldern. He was a prophet of the dais, passionate, angry, and importunate. He hammered us with phrases soon to become famous in the behavioral sciences: imprinting, ritualization, aggressive drive, overflow; and the names of animals: graylag goose, jackdaw, stickleback. He had come to proclaim a new approach to the study of behavior. Instinct has been reinstated, he said; the role of learning was grossly overestimated by B. F. Skinner and other behaviorists; we must now press on in a new direction.

  He had my complete attention. Still young and very impressionable, I was quick to answer his call to arms. Lorenz was challenging the comparative psychology establishment. He was telling us that most animal behavior is preordained. It is composed of fixed-action patterns, sequences of movements programmed in the brain by heredity, which unfold through the life of an animal in response to particular signals in the natural environment. When triggered at the right place and time, they lead the animal through a sequence of correct steps to find food, to avoid predators, and to reproduce. The animal does not require previous experience in order to survive. It has only to obey.

  Obedience to instinct: that formula has the ring of an old and tiresome story. Operant conditioning sounds so much more modern. But Lorenz strengthened his case with the logic of evolutionary biology, which secured my allegiance. Each species has its own repertoire of fixed-action patterns. In the case of a particular bird species, for example, the individual spreads its plumes in a certain way to attract mates of its own species; it bonds at a certain time of the year; it builds a nest of the right shape at the right location. Fixed-action patterns are biological events; they are not “psychological.” Having a genetic basis, they can be isolated and studied in the same manner as anatomical parts or biochemical reactions, species by species. They are prescribed by particular genes on particular chromosomes. They come into existence and change as one species evolves into another. They serve, no less than anatomy and physiology, as a basis for classification and the recon
struction of trees of evolutionary descent, which clarify the true relationships among species. Instinct, the great ethologist made clear to me, belongs in the Modern Synthesis of evolutionary biology. And that means you can take ethology out into the field and do something with it.

  Lorenz’s lecture and my supplementary reading in later months drew me in a new direction. The ethologists were giving shape to something I had tried to do earlier with the dacetine ants but for which I had lacked a theory and vocabulary. My thoughts now raced. Lorenz has returned animal behavior to natural history. My domain. Naturalists, not psychologists with their oversimple white rats and mazes, are the best persons to study animal behavior.

  The fixed-action patterns are what count, I realized. They can be understood only as part of the adaptation of individual species to a particular part of the natural environment. One kind of bird compared to another. One kind of ant against another. If you watch a chimpanzee in a cage, even if you test all its supposed learning ability, you will never see more than a small part of the behavior with which the animal is programmed, and you will miss the full significance of even that part.

  What made ethology even more beguiling was the principle that although fixed-action patterns are complex, the signals triggering them are simple. Take the European robin, an early subject of ethological analysis by the British ornithologist David Lack. The male, primed by springtime hormones, uses song and displays to chase other males out of his territory. If these warnings fail, he attacks the intruders with fluttering wings and stabbing beak. His aggression is not provoked by the whole image of a male robin as we see it. He vents his fury instead against a red breast on a tree limb. A stuffed immature male with an olive breast meets no response, but a simple tuft of red feathers mounted on a wire coil evokes the full response.

  Lorenz ticked off other examples of the triggering stimuli, or releasers as ethologists call them. The great majority of case studies accumulated by 1953 were of birds and fishes, and he concentrated on them. But the choice of these animals imposes a great bias: their communication is mediated primarily by sight or sound. It occurred to me immediately that the fixed-action patterns of ants and other social insects are triggered by chemicals instead, substances these creatures can smell or taste. Earlier generations of entomologists had already suggested something along this line; after all, such creatures cannot see in the darkness of their nests, and little evidence existed that they could hear airborne sounds. Some earlier writers had also believed that ants communicate by tapping one another with their antennae and forelegs, using a kind of Morse code of the blind. But in 1953 we knew nothing about the anatomical source of the chemicals that evoke the smells and tastes, with one exception—a hindgut trail substance, passed through the anus, found by the British biologist J. D. Carthy in 1951. Still, no one had located the ultimate glandular source of the molecules or identified their chemical structure. The idea of fixed-action patterns and releasers suggested to me a way to enter this unexplored world of ant communication. The method should, I reasoned, consist of a set of straightforward steps: break ant social behavior into fixed-action patterns; then by trial and error determine which secretions contain the releasers; finally, separate and identify the active chemicals in the secretions.

  As far as I knew I was the only person thinking along these lines. So I felt in no hurry to get started. In any case I had first to finish my Ph.D. thesis, a laborious exercise in anatomy and taxonomy of the ant genus Lasius. With that completed in the fall of 1954, I left for the South Pacific to launch my studies on ant ecology and island biogeography. Finally, four years later, back in Cambridge with a well-equipped laboratory, I began the search for the chemical releasers of ant communication. Even then the idea evidently still eluded others; I had plenty of sea room. It was to be a year before Adolf Butenandt, Peter Karlson, and Martin Lüscher introduced the word “pheromone” to replace “ectohormone” in the literature of animal behavior. They used the term “hormone” to designate a chemical messenger inside the body of the organism, “pheromone” for a chemical messenger passed between organisms.

  I started with the imported fire ant, my favorite ant species since my college years and one of the easiest social insects to culture in the laboratory. I devised a new kind of artificial nest consisting of clear Plexiglas chambers and galleries resting on broad glass platforms. The arrangement kept the entire colony in continuous view, allowing me to run experiments and record the responses of all the ants any time I chose. The ultrasimple environment did not distress the workers. After a while they habituated to the light and carried on their daily rounds in what appeared to be a normal manner. They flourished in an ant’s equivalent of a fishbowl.

  The most conspicuous form of communication in fire ants is the laying of odor trails to food. Scouts leave the nest singly to search outward in paths forming irregular loops. When they encounter a particle of food too big or awkward to carry home in one trip, most commonly a dead insect or a sprinkling of aphid honeydew, they head back to the nest in a more or less direct line while laying an odor trail. Some of their nestmates then follow this invisible path back to the food. As I watched from the side while the ants were foraging, I noticed that the returning scout touched the tip of her abdomen (the rearmost part of the body) to the ground and extruded and dragged her sting for short intervals along the surface. The chemical releaser apparently was being paid out through the sting like ink from a pen.

  Now I had to locate the source of the chemical, which I presumed to be somewhere inside the abdomen of the worker ant. To take this next step I needed to identify the organ making the chemical and use it to lay artificial trails of my own; I needed to steal the ants’ signal and use it to speak to them myself. The abdomen of a worker is the size of a grain of salt and packed with organs barely visible to the naked eye. Making the task more difficult was the fact that the anatomy of the fire ant had not yet been studied. I had to use diagrams drawn of other kinds of ants and add a bit of guesswork.

  After placing the severed abdomens of fire ants under a dissecting microscope, I used the tips of fine needles and sharpened watchmaker’s forceps to open them up and take out their internal organs one by one. I found myself close to the lower size limit of unaided dissection. Had the organs been only a fraction smaller, I would have been forced to use a micromanipulator, a difficult and expensive piece of equipment I hoped to bypass. If you buy instruments like that, and the experiment fails, you lose a lot of money. Although my hands were steady, I discovered that their natural muscle tremor, barely visible to the naked eye, was enlarged to a palsy under the microscope. Magnified twenty or thirty times, the tips of the needles and forceps spasmed uncontrollably as I brought them close to the abdomens. Then I found the solution: simply make the tremors part of the dissecting technique. Turn the needles and forceps into little jackhammers. Use the muscle spasms to tear open the abdomen and to push the separate organs out of the body cavity.

  This much accomplished, I washed each organ in Ringer’s solution, which is synthetic insect plasma with concentrations of various salts matching those in insects. Then I made artificial trails in the simplest, most direct way I could conceive, as follows. First I placed drops of sugar water on the glass foraging plate near the nest entrance and let mobs of feeding workers gather around them. With my experimental subjects in place, I crushed each organ in turn on the tip of a sharpened birch-wood applicator stick. Then I pressed the tip down on the surface of the glass and smeared the microscopic fleck of semiliquid matter in a line from the assembled workers outward in a direction away from the nest.

  First I tried the hindgut, the poison gland, and the fat body, which together fill most of the abdominal cavity. Nothing happened. In the end I came to Dufour’s gland, a tiny finger-shaped structure about which almost nothing was known. It empties into a channel at the base of the sting, the conduit known to carry venom to the outside. Might it contain the trail pheromone? Indeed it did. The response of the ants w
as explosive. I had expected a few workers to saunter away from the sugar-drop crowd to see what might lie at the end of the new trail. What I got was a rush of dozens of excited ants. They tumbled over one another in their haste to follow the path I had blazed for them. 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.

  That night I could not sleep. After a delay of five years my idea had paid off with only a few hours’ work: I had identified the first gland that contributes to ant communication. More than that, I had discovered what seemed to be a new phenomenon in chemical communication. The pheromone in the gland is not just a guidepost for workers who choose to search for food, but the signal itself—both the command and the instruction during the search for food. The chemical was everything. And the bioassay instantly became that much easier. It wasn’t necessary, I realized happily, to arrange delicate social settings with a multiplicity of other stimuli to get the desired result. Biologists and their chemist partners should be able to proceed directly to the pheromone’s molecular structure, provided they had an effective and easily measured behavioral test. If other pheromones—say, those inducing alarm and assembly—acted the same way as the trail substance, we might decipher a large part of the ant’s chemical vocabulary within a short time.

  Over the next few days I confirmed the efficiency of the trail pheromone assay over and over. In science there is nothing more pleasant than repeating an experiment that works. When I led my trails all the way back to the entrance of the nest, out poured the ants, even when they had been offered no food to stimulate them first. And when I let a concentrated vapor made from many ants waft down onto the nest, a large percentage of the worker force emerged and spread out in apparent search of food.