An epidemic of itchy, burning rashes, irritated eyes, and sore throats struck Belgium in the spring of 2007. Victims’ reactions were severe enough to rally firefighters and dozens of troops—armed with gas-flame torches—to scour the northern countryside in search of the culprits. That summer a similar outbreak in west London set people to coughing and scratching, and the U.K. forestry commission launched its own extreme counterattack to blunt a recurrence this year.
What’s responsible? Fuzzy caterpillars. Oak processionary caterpillars (Thaumetopoea processionea), to be exact: they wreak havoc on anybody unlucky enough to cross their path. Considered tree pests as well, because they defoliate oaks, oak processionaries sport an armament of poisonous hairs. The fine, stiff, sharp-pointed bristles readily penetrate skin, releasing a toxin on contact from their hollow cores. In response to the toxin, thaumetopoein, a victim’s body releases histamine, which raises itching, red welts. Particularly sensitive people can suffer a much more serious, life-threatening reaction termed anaphylaxis.
Surprisingly, few of the victims in the outbreaks actually touched or saw the caterpillars. The hairs can be unavoidable on a windy day, floating invisibly in the air for more than a mile. High concentrations of the airborne hairs are common because the caterpillars live in large sibling groups—often of a hundred or more—and can achieve high population densities. The caterpillars move about in head-to-tail bodily contact, forming snakelike lines as long as twenty feet, a peculiar form of collective locomotion termed processioning. While this is an effective means of staying together, brazen marches render the insects conspicuous to predators, requiring strong defense against attack. Hence, the hairs—lots of them.
People all over the world have come into contact with the dozens of species of processionaries that have evolved around the world. In West Africa, for instance, inhabitants have eaten the Anaphe caterpillar for many generations. They deal with the hairs by singeing them as the caterpillars are roasted over a fire. Eating one or two of the tasty caterpillars is of no concern. But making regular meals of them, it turns out, often leads to serious symptoms: difficulty in speaking, impaired consciousness, rolling eyes, staggering, and tremors. Only recently has it been established that thiaminase, an enzyme in the caterpillar’s body, destroys the victim’s vitamin B1. The resultant vitamin deficiency, now known as seasonal ataxia, was responsible for about 70 percent of?hospital admissions in Ikare, Nigeria, in August 1993. Fortunately, the symptoms disappear quickly with vitamin supplements.
The most dangerous of the processionaries is the South American Lonomia. In Brazil, a seventy-year-old woman suddenly fell into a coma after she placed a slipper on her foot. Hidden within was a Lonomia caterpillar. Doctors found lesions on her left foot where hairs had penetrated her skin. The toxin had triggered intracerebral hemorrhages, from which she died seven days later. More and more people are being exposed to the hazard because of deforestation and a decline in the caterpillar’s natural enemies. An antilonomic serum, if injected in a timely manner, can save victims’ lives.
Central America has suffered in recent years from female moths in the processionary genus Hylesia. The moth, like that of some other species of processionaries, has poisonous spicules on its abdomen, allowing it to carry on the nasty business of its childhood. In 2005, Trinidad shut down offshore oil rigs when the moths fluttered about lights that burned through the night; the spicules broke from their abdomens, drifted invisibly through the air, and fell onto the exposed skin of the victims.
Animals as well as humans fall victim to processionaries. Veterinarians are accustomed to treating curious pets that molest caterpillar processions or nests; the unfortunate animals often suffer necrosis of their tongues, requiring that affected parts be cut out to save their lives. In Australia, the processionary Ochrogaster is the prime suspect in a recent rash of aborted foals: there is growing evidence that if pregnant mares ingest fragments of hairs left behind as the caterpillars march over the ground, their fetuses may die. Although the exact mechanism remains uncertain, the hairs may irritate the mare’s gut, which allows pathogenic bacteria to invade the bloodstream.
While it is mostly because of their impact on human health that processionaries have attracted the attention of scientists, I was drawn to them for a wholly different reason. My interest was piqued after reading a series of essays on the pine processionary caterpillar (Thaumetopoea pityocampa) written more than a hundred years ago by the renowned French naturalist Jean-Henri Fabre. Fabre conducted remarkably detailed studies of the larva and the moth, which he recorded in his encyclopedic ten-volume Souvenirs Entomologiques.
In January 1896, Fabre wondered what would happen if the first caterpillar in a procession could be made to follow the last, creating a complete circle. He soon had his answer, for by chance a procession crawled onto a palm pot in his greenhouse and formed a circular procession around its rim. To his amazement the caterpillars circled for seven days before breaking free. Factoring in rest breaks during the cold nights, Fabre calculated, conservatively, that the caterpillars marched for eighty-four hours, circling the rim 335 times. He attributed the circling behavior to blind instinct, stating that the caterpillars lacked “the rudimentary glimmers of reason that would advise them to abandon it.” His account of the circling procession is one of the best known of all insect stories, because it is viewed as a metaphor for mindless living. The story has been endlessly retold by inspirational speakers who see in it the folly of blindly following the crowd, striking off with neither a goal nor a leader, or confusing activity with progress.
I pondered Fabre’s account, not from the point of view of one searching for inspiration, but from that of a scientist who had spent nearly all of?his working years investigating the behavioral and chemical ecology of social caterpillars. In truth, I doubted that caterpillars could be endlessly trapped in a circular procession merely because they adhered to an instinct to follow each other; something else was at work here. I also wondered, as had Fabre, how the caterpillars managed to form and maintain processions in the first place. Fabre observed that each caterpillar lays down a fine thread of silk as it marches along. Although he never formally tested his hypothesis, he felt that the caterpillars sensed those strands, leading them to trail one behind the other. Fabre was an acute observer, but he died long before the discovery of the role of pheromones in orchestrating the collective behavior of social insects. My research with other species of social caterpillars suggested that a previously undetected pheromone might be essential to the formation of processions. Thus, I set off on a study of the behavioral ecology of the pine processionary, which lives in southern Europe and northern Africa.
When I initiated my investigation, I was fully aware of the caterpillar’s toxic nature. Insatiable experimenter that he was, Fabre reported that he suffered severe rashes when he poured extracts of the caterpillar onto his skin. One of his contemporaries, attempting a similar experiment, experienced a much more dangerous anaphylactic response and reported that “not only my hands, my arms, my legs, but my whole body became the seat of insupportable itching; soon my face swelled, my eyes puffed up and I had to give up writing my remarks.” After suffering a severe conjunctivitis when a tiny fragment of a caterpillar’s hair fell onto my eye, I found it necessary to move with caution in the field and to confine the caterpillars in my laboratory to a room fitted with air filters. Nonetheless, there were few days during my studies when I didn’t have to deal with an itching dermatitis.
I conducted my field studies in Catalonia, Spain, where the life cycle of the pine processionary begins in early August, when the moth lays up to 300 or so eggs on pine needles. Soon after they hatch, the tiny caterpillars construct a flimsy silk nest around a few pine needles. That nest is abandoned after a short while, and over the next month the caterpillars collectively build a succession of nests at new sites in the branches of the tree. Their nomadic nesting habits end after their second molt, when they initiate the construction of a dense and virtually impenetrable silk nest they will inhabit for the rest of their larval lives. The permanent nest stands apart from the caterpillar’s food supply, and they march from it to feeding sites on the host tree, returning home hours later with full guts. It is with the initiation of the permanent nest and the long marches that the caterpillars’ hairs, until now soft and harmless, grow into stiff, toxic bristles. Their nest becomes littered with those bristles, fortifying it against attack by would-be predators.
A striking feature of the pine processionary’s life cycle is that the insect spends the winter in the caterpillar stage. Since insects are ectothermic, producing no body heat, one would expect that they would lie immobilized in their nests on cold winter days. To determine how the caterpillars fared during winter, I set up activity monitors near nests in mid-February. The monitors projected invisible infrared beams across pathways the caterpillars used when they foraged. When the beam was interrupted by a passing caterpillar, the signal was sent to a data logger, time-stamped, and later uploaded to a computer for analysis.
During the week of my study, temperatures in the afternoon reached average highs of 63 degrees Fahrenheit, but plummeted rapidly to below freezing after sunset. Yet the monitors revealed that the caterpillars only left their nests after dark and returned before dawn. One morning I observed that water had turned to ice in a pot left outside overnight, and I was sure I would find that the caterpillars had spent the previous night snug in their nests. But the data loggers revealed that they had been active outside their nests until the temperature dropped below 28 degrees, at which point they became immobilized. As soon as the first rays of the morning sun struck them, their bodies warmed, allowing them to make their way back to the nest, and by 9 a.m. all were home.
The study revealed that the caterpillar has one of the lowest “chill-coma” temperatures (the temperature when all activity ceases) ever documented for an insect. It is likely that selection pressure from daytime predators accounts for that seemingly strange behavior. For not all predators are put off by the pine processionary’s toxicity. Remarkably, the hoopoe, the great tit, and the great spotted cuckoo are all able to feed on the caterpillars without ill effect.
Although the nest serves as a secure retreat, it has another equally essential function. During sunny days, it traps solar radiation. Thermo-sensitive probes I placed in nests in February registered as high as 100 degrees during the day. Heat trapping warms the caterpillars enough during even the coldest days to enable them to efficiently metabolize the food they’ve collected during their nightly forays.
In early March the caterpillars take their last meal, an event followed by a grand procession. Up to now they have confined their forays to the host tree, but on this occasion they march down to the base of the tree and set off over the ground in a snaking procession. The leader advances, goaded on by the mass of caterpillars that push from behind. The caterpillars are in search of a place to spin their cocoons. Along the way they test the ground, seeking loose soil, and eventually they bury themselves side by side several inches underground to undergo metamorphosis. The timing is right because the nests would be much too hot to occupy in the torrid summers that characterize much of their range. The pupating processionaries stay underground until August, when, as moths, they burrow up through the soil [see illustration below]. Children who uncover one of the communal crypts while digging in sand in the summer become inadvertent victims of the caterpillars’ hairs. The abandoned nests, too, continue to spew toxic particles into the air well into the summer.
Pine processionary moths lay eggs on the needles of pine trees every August. When the young larvae hatch, they construct and abandon a succession of small nests at different spots on their home pine tree. After two molts they build a large, permanent nest (center) that is formidable to intruders, thanks to toxic hairs strewn throughout, and that provides good shelter through the winter. In March the caterpillars leave their nest in search of a site where they can bury themselves underground, spin cocoons, and metamorphose.
My goal was to determine how the pine larvae are able to maintain their orderly processions. First off, I found that the caterpillars left behind a persistent trail. I did this by marking the precise course of a procession with pins and then releasing single, uninitiated caterpillars along the pathway. That simple test revealed that individual caterpillars followed the procession when released as long as a full day after the procession had passed.
Next I tested Fabre’s hypothesis that the strands of silk the caterpillars lay down as they march are the basis for the trail: I temporarily plugged the tips of the silk-spinning apparatus, the spinneret, of each member of a group of caterpillars. That had no effect on their ability to line up and follow one another, or on the ability of a caterpillar introduced to the trail hours later to follow its path. The trail was an invisible one.
Further investigation revealed, as I had suspected, that processionaries mark their pathway with a pheromone secreted from the underside of their abdomens. When I sealed the suspected site of pheromone secretion, as well as the spinnerets, the caterpillars did not leave a persistent trail that a lone latecomer could follow. Nevertheless, they still formed and maintained processions. That suggested tactile stimulation—caterpillars brushing each other from behind—was the ultimate basis for the formation and maintenance of processions. To test that, I had to sacrifice a caterpillar and pull its eviscerated skin over the end of small stick, making a model of a caterpillar. With the model, I found I could lead a procession in any direction by moving it slowly in front of the leader. Moreover, I was able to do the same with a model made from a completely unrelated species of caterpillar.
If tactile stimuli alone are adequate to allow the caterpillars to march in line, what then are the functions of the silk pathway and the trail pheromone? I concluded that the sticky silk, bonding to the smooth branches of the host tree, gives the caterpillars’ feet extra traction. And the persistent pheromone serves to guide the caterpillars back to the nest after their nighttime feeding foray (and also enables laggards to catch up). The caterpillars discriminate between old and new pheromone trails and between trails made by different numbers of individuals. That facilitates efficient and coordinated movement between the nest and distant feeding sites.
During their final over-the-ground procession, however, the caterpillars rely solely on tactile stimuli to stay together. (The leader has no foreknowledge of where to go, but may use the Sun for direction.) I learned this by rapidly removing single, centrally located caterpillars from their places in line, dividing processions in two. The new leader of a rear contingent would swing its body in a frenetic search for the caterpillar that had been snatched away, then end up striking off independently in a new direction. None succeeded in bridging the gap I had created. Either the caterpillars do not lay down a pheromone trail during these terminal marches or the rough terrain renders it too spotty to be a useful guide.
And what of Fabre’s caterpillars that circled endlessly around the rim of a pot? My suspicion was that the caterpillars were not adhering blindly to their instinct to follow each other, but were in effect physically trapped on the rim. I tested this by arranging for caterpillars to make a circular trail on a flat surface rather than on the rim of a pot. I placed seventeen inside a circular arena on a tabletop. The caterpillars soon arranged themselves against the wall of the arena and commenced marching in an unbroken, head-to-tail circular procession. After half an hour I removed the arena, freeing the caterpillars from any physical constraint. If Fabre’s interpretation had been correct, the caterpillars should have continued to circle for days, or until they grew exhausted. But in fact, they continued in a circle for a short time (on average in my experiments, only two minutes), then marched off in a straight line. When I tried the same experiment with caterpillars younger than those used by Fabre, I learned that the young ones are more dependent on the trails. Their circular processions lasted an average of two and a half hours. One group circled continuously for twelve hours—a remarkable performance, but far short of the seven days.
But what does keep caterpillars marching around a rim? I once climbed the ninety-one steps of the Temple of Kukulkán at Chichén Itzá and found, as have many others, that going up the steep staircase is much easier than coming down, which is quite scary. Fabre’s circling caterpillars likely found themselves in a similar predicament, weighing their secure footing on the rim of the pot against a plunge down its steep and smooth sides. In one famous case of similar entrapment, the New York Times reported that in June of 1913, teeming hordes of another social species, the forest tent caterpillar, climbed onto the tracks of the Long Island Rail Road. Rather than go up and over, the caterpillars showed the same reluctance to descend as had Fabre’s. The rails were soon covered with the slippery remains of tens of millions of caterpillars, until eventually the wheels of locomotives spun in place!
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