The Case of the Vanishing Caterpillar

A butterfly larva’s fate depends on who finds it first—its ant friends or ant foes.

The metamorphosis of Ross’s metalmark takes eleven days. The process begins with the Anatole chrysalis in its chamber, attached to the subterranean portion of the croton stem or to its root. Although the organism does not produce honeydew in this stage, it does possess glandular openings corresponding in position to the pheromone-producing organs of the caterpillar, and I conclude that a similar chemical is released into the air. At any rate, the ants remain in the pen for nine days—until two days before the butterfly’s emergence. Then, as the adult form nears perfection, its pheromone glands atrophy. The ants depart, leaving the pen open. The butterfly later emerges from the old pupal skin, climbs out of the darkness it has inhabited during the daylight hours for nearly two months, and enters the bright, sunny world of the pine ridges. After an hour or so of drying and exercising its newly formed wings, the butterfly departs for a free, aerial existence, which it enjoys for as long as a month, apparently oblivious to its past ant associates.

Many questions arose in the course of my observations. Do the ants remain with their charge throughout its development or do they sometimes return to their nest site? What would happen if the caterpillars were isolated from their ants? Is the association between ants and caterpillars of benefit to both species?

I experimented. First, I carefully opened a pen, and taking out the ants one by one, I dabbed each on its back with a drop of quick-drying paint. I repeated this procedure with four nearby pens, using a different color for each. Three days later I observed that all of the painted ants had either been replaced by unpainted ones or else had moved to different chambers. There evidently was a changing of the guard as the ants circulated to and from their central nest and over their territory. Eventually I learned that the ants’ nest may be up to fifty feet away, its inhabitants exploiting a variety of resources-saps, flower nectars, and other sweets. The caterpillars seem to be just one source of food they encounter. The ants’ response-secreting the unwieldy prize in a hole instead of attempting to carry it back to the nest—may not have been specifically evolved to cope with the Anatole caterpillar. Similar behavior has been observed in several species of ants. The herding behavior may be a more specialized feature of the ants that evolved in association with these caterpillars.

In another experiment I removed the attending ants from several crotons and placed net cages around the plants to keep them out. When thus isolated from their caretakers, the caterpillars did not return to their subterranean cells after feeding but, instead, remained on the leaves and fed intermittently throughout the day and night. Evidently the daily journeys up and down the plants were forced on the caterpillars by the ants.

Then I removed several caterpillars and placed them on croton plants that were outside the butterfly-caterpillar colonies. Left unattended, the caterpillars were invariably attacked by workers of Ectatoma tuberculatum, large reddish ants festooned with numerous hairs and spines. This species is a member of a widespread group of ants, the Ponerinae, known for their fierce stinging ability and voracious predatory habits. The Popoluca’s name for this species translates as “the robbers,” appropriate for sinister-looking creatures that are frequently seen carrying assorted insect prey to their tree-hole nests.

A newly emerged Ross’s metalmark butterfly dries its wings.

I was personally well acquainted with Ectatoma. Just a few days prior to my relocation experiments, I had been stung on the thumb as I leaned against an oak tree. My finger was numb for nearly twenty-four hours and swollen for another day. I could imagine the damage such a sting would inflict on a caterpillar. I have since learned that, when stung, a larva undergoes extensive tissue destruction within a few minutes.

The relationship between the carpenter ants and the metalmark caterpillars thus appeared to be one in which the larvae furnished the ants with tasty sweets and in return received protection from a vicious armed predator, another ant species. To confirm this, I carefully investigated the pine ridge crests and upper slopes, exclusive habitats of the metalmark butterfly. The Ectatoma ants infested these open areas and spent the daylight hours solitarily stalking potential prey. At night, however, they remained secluded in their nests. The Anatole caterpillars and their wood ant guardians were prime targets, but they were hidden beneath the ground during the day when the predators were on patrol. At night, with the plundering halted as the Ectatoma ants stayed in their own nests, the caterpillars could feed in complete safety, exposed on their plants. Therefore, the relationship between the carpenter ants and metalmark caterpillars is mutually beneficial. Biologists call such a symbiotic relationship, in which both parties benefit, mutualism.

There is one other chapter to this story. During the cooler months of winter and early spring, the ant-caterpillar activities are somewhat altered. Between November and April, nighttime temperatures may drop to 50°. Adult butterflies are no longer on the wing, having died as the cool, damp weather set in. The ants deepen the pens into five- to six-inch vertical tunnels, probably to increase insulation from the cold air. The butterfly’s larval stage is greatly lengthened as the caterpillars and their attending ants become sluggish. Frequently a caterpillar will crawl up a plant during the early night hours, take a few bites, and then be herded immediately back into the pen. At times, particularly during very cool spells, the caterpillars do not emerge at all for many consecutive nights, presumably able to subsist on stored nutrients because of a reduced metabolism.

As spring, with its warmer temperatures, begins in the Sierra de Tuxtla, so does the dry season. Much of the undergrowth in the various ecological communities rapidly withers and dries. At this time, humans become an important factor in the perpetuation of the metalmark’s life cycle. The Popoluca men toss lighted matches alongside the numerous trails on the pine ridges adjacent to their villages. The pine needles and dried undergrowth make excellent tinder, and the flames spread rapidly along and down the ridges. Because the ground is only sparsely covered, there is no widespread inferno, only low ground fires that creep in irregular patterns. The goal of this annual activity is to clear clutter from the ground in order to encourage the growth of fresh grasses that will serve as fodder for mules, burros, and horses. This allows the work animals to be pastured only short distances from the Popoluca villages.

By mid- or late April, selected sections of the pine ridges—and practically all butterfly-caterpillar colonies—have been burned over. However, because the wood ants previously deepened the pens during the cool months, the fires do not harm the secluded insects. They emerge the night after the firing and find a new world, one devoid of food plants and littered with burned debris. The absence of food for these winter-season caterpillars now triggers the onset of their long-delayed pupal period. No more than twelve days after fire passes through a colony, all the caterpillars transform into chrysalises. In two more weeks—by late April or early May—a fresh generation of butterflies is flying about.

Soon mating occurs and the females begin to lay their eggs. They select only the small shoots of croton plants that have recently sprouted from the bare, scorched patches of ground near their original larval food plants. The newly emerged cr0tons look much healthier than others growing in unburned localities. They are shorter, brighter green, and have relatively smooth leaves. The butterflies instinctively avoid placing their eggs on larger, more spindly plants with hairy leaves. While rearing caterpillars in my field laboratory, I observed that the young larvae could not penetrate the velvety surface of these larger plants; they soon became emaciated and died, presumably from starvation.

Ross in Mexico in the early 1960s

The distinctive growth form of the crotons in the metalmark colonies may be a response to the increased sunlight that pours into the burned-over areas. In unburned, grassy areas, even new-grown crotons produce hairier leaves. This difference, so important to the young caterpillars, remains in effect throughout the year. Thus, both the spring burning carried out by the villagers and the selectivity of the egg-laying butterflies insure colony stability and are critical to the survival of the species.

With the successful reproduction of the “spring crop” of butterflies, the cycle closes. Ross’s metalmark seems to reproduce exclusively in an environment that is hostile to most other defenseless insects. It lives and breeds in a tiny habitat—pine ridges close to Popoluca Indian villages—that is burned regularly and systematically by the indigenous population and is the hunting territory of a potentially devastating ant predator. The butterfly thrives, where others cannot, because of its pact with a specific wood ant—a pact that, if somehow broken, would almost surely spell the butterfly’s immediate extinction.

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