A Farming Ant and Its Fungus Are Ancient Cohabitants

by Natalie Angier
from the Science Times, New York Times
Tuesday, December 13, 1994

They are tiny mandibled versions of Shiva, the Hindu god of devastation and restoration. In a mere three days, they can strip away every last trembling leaf, every vestige of chlorophyll from a large grove of trees. A herd of elephants or a blazing inferno could hardly do more damage to the face of a forest. Yet once they take their herbaceous plunder underground, the pillagers become gentle farmers, using the leafy matter to cultivate vast gardens of blooming fungi. They nourish the fungus, and the fungus in turn feeds their hungry multitudes.

And so the famed leaf-cutting ants act out their high drama of destruction and renewal, defoliating trees, bushes, vines, everything in their path?and from the wreckage creating a subterranean Eden, a myrmecian paradise.

The leaf-cutters represent the most advanced division of a powerful insect tribe called the attine ants, 200 species that engage in a mutually convenient arrangement with fungi. The ants and the fungi are symbionts, dependent on one another for survival and each having evolved specializations to optimize their intertwined existence.

The ants offer the fungi huge amounts of material that they gather from their surroundings, far more than the sedentary fungus could engulf on its own; and the fungus mulches the biomass and grows so fat that its hyphal tips swell with nutrients, sugars and protein, on which the ants can nibble.

Scientists have long been impressed by the harmony of the partnership between attine ants and their colluding mold. And what scientist could ignore the ants spectacular gardens when in building them the insects displace enough earth to fill a good-size human living room? Yet only now are biologists discovering the nuances of the relationship and the evolutionary history behind it.

They are applying molecular tools to reconstruct the genealogy of the symbiosis, determining when it arose and how it progressed over millions of years to assume, in its peak among the leaf-cutters, a partnership so powerful that it virtually controls the ecosystem of many regions of the Neotropics.

Dr. Edward 0. Wilson, a naturalist at Harvard University and author, with Bert Holldobler, of the acclaimed book "The Ants," has described the adaptation of ants using fungi to take advantage of fresh vegetation as so successful "that it can be properly called one of the major breakthroughs in animal evolution."

In two papers appearing in the current issue of the journal Science, researchers describe a number of complexities of the ant-fungal affair. They demonstrate that the co- evolution of the attine ants and their fungi dates from 50 million years back, reaching varying degrees of co- dependency in each case. Among the leaf-cutters, the relationship turns out to be so tightly linked that the ants have relied on a clone of the same fungus for 25 million years, with each new colony sowing its first garden with a bit of starter fungus from the parent nest. This means that every fungal crop found on every leaf-cutter's farm throughout South and Central America, where the ants thrive, is a descendant of a single ancestral spore.

To the relief of mycologists, the researchers have solved a century old mystery experts had not been able to determine the fungal variety through a traditional taxonomic analysis of the fungus's fruiting body - the cap of the mushroom, where the spores are found. In becoming a symbiont with ants, the fungus had ceased making fruiting bodies to reproduce itself and instead had come to rely on the insects to spread their seed around.

Now, by examining genetic sequences of fungal samples taken from the gardens of many of the attine species, the scientists have concluded that most of the molds are of the family Lepiotaceae, which claims among its members the parasol mushrooms familiar to connoisseurs and pickers and not all that different from the little white mushrooms sold in supermarkets everywhere.

The scientists also demonstrate that while members of the leaf-cutting branch of the attine tribe have become near- monoculturists, generally slicking with one very ancient strain of fungus to feed upon, those in another group of the ants are more supple in their agriculture techniques, occasionally acquiring new fungi from the outside to refresh their stocks and perhaps provide a variety of flavors in their diet. The more omnivorous ants are considered the more ancient or primitive types, closer to the founding fungal farmers that shopped around for the best spores to exploit in their gardens.

"This is what it must have been like 50 million years ago when this symbiosis was just getting started," said Dr. Ulrich G. Mueller of Cornell University, the senior author on one of the Science papers. "It wasn't a single acquisition event, but rather something that happened over a period of time as the ants were driven into the role of associating with fungi.

The new work is of interest on multiple counts. Scientists now have a better handle on the symbiosis between ants and fungi than they do about most of the other mutualistic arrangements between natural organisms, of which there are many. Mycologists celebrate the research for its emphasis on fungi, which are of fundamental importance to all ecosystems on land and yet which are so robustly ignored that most universities do not bother having a mycologist on their faculties.

"Fungi are more numerous than plants by sixfold, yet there are a tenth the number of people studying them," said Dr. Thomas Bruns, a mycologist at the University of California at Berkeley. "That's starting to change as ecologists recognize that fungi are the basis of all terrestrial ecosystems. These papers add a lot of wonderful new data to the fungal sequence banks." Mycologists emphasize that ants are far from the only organisms to discover the advantages of cooperating with fungi. Many plants, for example, rely on fungi growing at the base of their roots to take up needed nutrients from the soil.

Ecologists also point out that the research underscores the interdependency of life, serving as yet an other reminder that habitats are composed of threads so tightly woven together that to yank out one stitch could lead to the unraveling of entire chains of life.

"Many organisms are involved in a community structure, and if an insult to the environment hurls or changes one element of that community structure, that could result in the loss of the capacity of the community to survive," said Dr. Mitchell L. Sogin of the Marine Biological Laboratory at Woods Hole, Mass., the senior scientist on the second paper in Science.

He also emphasized that microorganisms like fungi often are symbiotic with macroorganisms like animals, and that any discussion of biological diversity must include an appreciation for the invisible among us. Where would humans be without the microorganisms in their gut that help digest food, he said, or for that matter, without the mitochondria in their cells, the powerhouse structures in the interior of cells that supply energy for the body and that are thought to have once been free living bacteria-like organisms?

Understanding the relationship between fungi and attine ants may also have practical applications. Leaf-cutters in tropical countries are essential to recycling plant material and to keeping the soil aerated as earthworms do in more temperate climates. Yet they are also a menace to humans who try to farm in tropical regions of the New World.

"Leaf-cutting ants are the dominant herbivore in the Neotropics, taking about 20 percent of all the fresh-leaf biomass there," said Ted R. Schultz, a graduate student at Cornell who was an author on both papers in Science. "It would be fair to say that the ants are the main reason it's hard to do agriculture in the Neotropics."

Most of the plants native to the Neotropics have evolved sufficient defenses that they are not entirely torn apart by the ineluctable energies of the attine ants, he said, but when people try to bring in foreign crops - fruit trees from California or Africa, say - the results are disastrous. "They'll strip entire orchards in no time," Mr. Schultz said.

North American farmers do not have the same concern about trying out foreign plant species, for although attine ants live as far north as Long Island, these species are of a less ambitious variety, and they feed their fungi less desirable goods, like insect feces or dead-leaf material.

In performing the current analysis, the researchers took genetic samples from 21 fungi isolated from the nests of 19 different types of attine ants and compared those genes with the DNA of free-living fungi not beholden to any ants. They also linked the genetic information from the fungi with previous analyses that had been performed on the molecular history of the attine ant tribe.

After subjecting the data to a series of elaborate statistical calculations the scientists came up with phylogenetic trees showing divergences among the ant species and their fungal mates. The results led the scientists to conclude that the more primitive ants pick and sample new fungi from the environment while the most highly specialized species remain unerringly faithful to the fungus that has served them so well.

The reason the leaf-cutters have stuck with their fungal strain is that the fungus can do what most fungi cannot: break down fresh leaves into usable nutrients. This means that a resource most herbivores find too daunting to nibble was laid open to the ants. Although incapable of digesting the leaves themselves, they could feed it to the fungus, allow the fungus to metabolize.e the material and then gorge themselves on the nutritious upwellings of the fungus. The beauty of the system has allowed leaf-cutters to evolve into the paradigm of what Dr. Wilson calls a "superorganism," a collection of individual ants that are each as specialized in their tasks as the cells of the body and that jointly perform the task of keeping the nest alive.

And what a nest it is. Those who study leaf-cutters in the tropics describe a leaf-cutter farm as a spectacle almost beyond belief. A mature nest may contain eight million ants, ranging in size from the tiny tenders of the fungal garden that are each no bigger than a letter on this page, to the pulsating, egg-swollen queen, which is the size of a whole, unshelled peanut. Most of the nest is underground, an elaborate warren of thousands of chambers ranging In size from a fist to a soccer ball, and all having been excavated by the ants. The chambers are filled with the spongy gray hyphae of the fungus that feeds all.

Above ground, the area surrounding the nest is kept scrupulously clean, tended by janitorial workers that will whisk off any leaf, any interloper, any bit of undesirable mold that may slow the ceaseless passage of the cutter ants heading to and from the farm. The gatherers of plant matter, each about the size of a housefly, venture out to slice leaves into crescent-shaped bits, which they hoist back to the plantation. In industrial, assembly-line fashion, the crescents arc taken up by smaller ants that slice the slices smaller still, and then pass the pieces along to yet tinier ants that chew the material and soften it with enzymes into a moist paste. Even smaller ants then spread the paste like a slathering of jam over the fungal substrate. The mold then takes over and does the rest, threading its hyphae tentacles through the plant matter and breaking down cellulose into nutrients the ants can use.

The fungus is pampered like a pet, fed to fatness and kept clean of competing microorganisms that might threaten the crop. As long as there are leaf-cutters, the lepiotaceous mold will thrive, for no virgin queen leaves home on the wing without first tucking a bit of it into her mouth to seed an estate of her own.
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