by Susan Lumpkin and Stephanie Hsia
When anthropologists look to the animal world for insights into human behavior, they usually focus on our closest relatives—chimpanzees and other primates. But scientists who study human agriculture go to much more far-flung branches on the tree of life to find other farmers, all the way to ants and other invertebrates a subphylum away.
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| This Atta cephalotes is one type of leafcutter ant that grows crops of fungus in its nest. (Scott Bauer/USDA ARS) |
Ants, termites, and beetles were farmers long before people began to plow the Earth. Some 40 to 60 million years before people started to cultivate plants for food, these insects evolved the ability to cultivate fungi for food. About 330 species of Old World termites farm fungi. Workers forage on wood, leaves, and grasses, which pass undigested through their bodies and come out as feces for the fungi to grow on. About 3,400 species of farming beetles, called ambrosia beetles, burrow into trees and create fungal gardens in them. But it is in the ants that insect agriculture reaches a degree of sophistication and complexity that rivals our own.
The Insect Farmers
Thomas Belt was a 19th-century British mining engineer
whose avocation was natural history. Stationed in Nicaragua
from 1866 to 1872, Belt detailed his observations of
this Central American country's natural history in an
1874 book called A Naturalist in Nicaragua,
a book that won high praise from no less a personage
than Charles Darwin. Ants figure prominently in the
text. In his efforts to rid his garden of leaf-cutting
ants, which entailed his careful study of their habits,
he hit on how they used the slivers of green leaves
they so assiduously carried into their underground nests.
Noting that others had guessed that they ate the leaf bits, or roofed their nests with them, Belt then wrote, "I believe the real use they make of them is as a manure, on which grows a minute species of fungus, on which they feed;—that they are, in reality, mushroom growers and eaters." He was right, and his amazing insight has inspired scientists to explore this ancient agricultural system for more than a century.
The first attine agriculturalists appeared more than 50 million years ago, eventually diversifying into more than 210 species within 12 genera of attines today. The attines are separated into two groups with distinct characteristics. Among other differences, lower attines use a variety of materials to fertilize their fungi, from dead insects and feces to fallen leaves and grasses. Their colonies are small and typically house a few hundred members living in a single garden. In contrast, higher attines, which include the leaf-cutter ants in the genera Atta and Acromyrmex, use only plant material to fertilize their fungi.
Predominately distributed in the Neotropics, fungus-growing ants play an extremely important role in the ecology of that area. Leaf-cutter ants and other higher attines, which comprise about a fifth of the species in the attine group, are the dominant herbivores in those ecosystems. Lower attines are major recyclers in the forest because they decompose and return nutrients underground. These numerous ants excavate deep into the earth and improve soil quality by introducing organic material and nutrient-rich waste products. The attine ants are so abundant in the Neotropics that, according to entomologist Ted Schultz of the Smithsonian's Museum of Natural History, a world authority on the subject, "If you had x-ray vision and looked out into the forest, you would see a number of fungus gardens in every cubic meter of soil."
Life Cycle of Leaf-cutters
A leaf-cutter ant farm, such as one of the Atta
species, begins with a single homesteader. A virgin
queen leaves the colony she grew up in and within a
few hours mates several times in order to gather enough
sperm to fertilize millions of eggs. If she survives
this short but risky phase of her life—and many
females do not—she then digs a little nest into
the soil to begin her new life. Along with a lifetime's
worth of sperm, the queen has other precious cargo.
Like a pioneer with a sack of seeds for her first planting,
she is carrying a gob of fungus lifted from a garden
in her natal colony and stored in a special cavity behind
her esophagus called an infrabuccal chamber.
In the small single room of her new nest, the queen spits the fungus gob onto the ground, and her first garden begins to grow. In a few days she will start laying eggs and soon her first brood of eggs and larvae will be sheltered in a large mass of fungus, from which the first adult worker ants will hatch. Until they do, the queen is a very busy ant. She tends her eggs and feeds other eggs to herself and her larvae. And all the while she is cultivating her garden, regularly plucking a small piece of fungus, fertilizing it with her liquid feces, and then replanting it in the garden. As soon as the first workers begin to forage outside the nest and tend the garden, care for eggs, and feed fungus to the larvae, the queen quits working and spends the rest of her life—as long as ten years—doing nothing but laying eggs while her colony grows to immense proportions.
Leaf-cutter worker ants forage for leaves, woody material, and detritus and carry them back to their nest. Other ants remove the leaves' waxy coating and chew them into a pulp. Then they insert the material into the garden substrate and, as the queen once did, pluck a bit of fungus and plant it in the prepared bed. Workers also manure the garden with their feces.
But preparing the field, planting, and fertilizing are only part of the ant farmers' chores. Attines have evolved other behaviors that make them effective fungiculturists. Worker ants patrol the garden, performing endless chemical inspections with their antennae. Before they add new garden substrate, they lick it to rid it of any alien microbes. If this preventative effort doesn't do the job and a fungus pathogen is detected, the ants groom the fungus. They remove alien spores with their mandibles and take them to a dump chamber, used specifically to stash unwanted material. If the fungus pathogen germinates, attines weed the garden and remove the substrate that contains the pathogen. The various tasks are performed by different types of workers—some cut, some groom, and others carry.
The parallels with our own agricultural system are obvious. The insects cultivate fungi within certain genera, and can switch the type that they grow. They protect their gardens from pathogens and remove undesirable organisms such as mites and nematodes by constant patrolling and weeding. And recently, they have been found to use an antibiotic to suppress pathogens, just as we use pesticides and insecticides to get rid of pests.
For more than a century after Belt, it was widely believed that there were only two players in this system—ants and fungi. But in 1997, Cameron Currie, then a graduate student at the University of Toronto, became suspicious that what had been previously described as a "waxy whitish bloom" on the bodies of the ants was actually bacteria. He wondered how the ants were so effective in keeping their gardens clean and free of pathogens. Currie and his colleagues conducted an extensive study of fungal gardens and discovered that the gardens were not, as traditionally believed, parasite free, but were commonly afflicted by a virulent pathogen fungus in the genus Escovopsis, a "weed" found in ant gardens and nowhere else. In the process, he also discovered a symbiotic bacteria that produces an antibiotic that specifically suppresses the growth of Escovopsis. The addition of the pathogen fungus and the antibiotic-producing bacteria makes the attine-fungi-bacteria system the most complex symbiosis ever discovered.
Origins of the Symbiosis
At the Natural History Museum's Department of Systematic
Biology, Ted Schultz is doing research to understand
the phylogenetics, or evolutionary history, of fungus-growing
ants. A leading authority on ants, Schultz collaborates
with behavioral ecologist Ulrich Mueller, microbial
ecologist Cameron Currie, and myrmecologist Stephen
Rehner. By looking at morphology and analyzing DNA,
Schultz is able to assemble species onto phylogenetic
trees that show how species are related. He has created
three charts depicting the ants, the fungi they cultivate,
and their parasitic fungus, and has detected patterns
across the trees.
"But there still remain major pieces of the puzzle to fulfill," Schultz says. The recent discovery of the antibiotic-producing bacteria has raised a plethora of questions. How did the ants first start using these bacteria? How do they promote the bacteria's growth, how does the bacteria benefit from the association, and why has natural selection favored this association?
The bacteria belong to a group called actinomycetes, which are commonly found living freely in soil. We derive many of our own antibiotics, such as streptomycin and tetramycin, from actinomycetes. The bacteria are passed on from adult ants to offspring, are concentrated on the underside of ants' bodies, and are more abundant on those workers tending the fungus gardens than workers performing other tasks. Cameron Currie and colleagues also demonstrated that the bacteria are specifically geared toward suppressing Escovopsis and do not have a large inhibitory effect on other fungi.
While scientists are in their first stages of understanding the relationship between ant and bacteria, they are further along in regards to ant-fungi symbiosis. Ants can farm many types of fungi and, though each colony maintains a single culture in its nests, an ant species usually cultivates two to eight different fungus species. Numerous theories have been proposed in the past as to which—the ants or the fungi—got the whole symbiosis started. The current theory Schultz and his collaborators are favoring is that the fungi were the ones that first started hitching a ride with the ants as a means of dispersing. Plants, and some other fungi, regularly use ants and other insects as dispersal agents. But, more data are needed.
There has been a surge of interest in studying attines in the past 15 years and new technologies have helped speed up the progress. Molecular techniques such as DNA sequencing have revealed much about the ecology of the fungi. Schultz and his collaborators have found two free-living fungi that are a 100 percent DNA match with fungi in ant colonies. This means that there have been recent domestication events in which ants have brought back with them free-living fungi from the wild. Moreover, ants of different and distantly related species sometimes share identical cultivars of a fungus, suggesting that one species may acquire its domesticated fungus from another. As Schultz writes, "The best long-term evolutionary strategy for most ant farmers seems to be cultivating a diversity of crops, rather than committing exclusively to a single one."
However, domestication of fungi may have occurred only once in the higher attines, whose fungal cultivars may be clones as old as 23 million years. In other words, the higher attines farm monocultures, and this may make them more susceptible to the attacks of the specialist Escovopsis, which can be suppressed by chemical means but sometimes escapes the ants' defenses and devastates a colony. Currie and his colleagues note the analogy to human agriculture: Widely planted cultivars with little genetic diversity are susceptible to epidemics, with sometimes horrific consequences for farmers who grow them to the exclusion of other food crops. The Irish potato famine of the mid-1800s is a classic example.
Proto-farming: Snails and Such
Recently, another invertebrate has been added to the
insect-farmer fold. Marsh snails (Littoraria irrorata),
which are abundant in salt marshes along the southeast
coast of the United States, primarily live on fungi
that grow on dead plant material but they also were
recently observed grazing on live cordgrass (Spartina
alterniflora). According to a study by ecologists
Brian Silliman and Steven Newall published in the Proceedings
of the National Academy of Sciences in 2003, the
snails do not, however, actually eat the live plant
material but dine on the fungi growing on cordgrass
leaves. But the leaves don't just serve up this food
on green platters. Instead, the snails use their radula—a
tonguelike organ—to cut wounds into leaf surfaces,
enabling fungi to invade and thrive in the wounds. In
fact, Silliman and Newall found that, compared to uninjured
leaves, wounded leaves carried 15 times more fungi by
weight.
The snails also appear to actively promote the fungi's invasion of the wounds by depositing their fecal pellets, which are full of both nitrogen and fungal hyphae, on the wounds. In the same study, adding fecal pellets to leaves with experimentally induced wounds increased the weight of fungi by 171 percent! Moreover, lab experiments revealed that snails grew hardly at all on uninjured leaves—and nearly half of all juveniles tested died on diets of uninjured leaves—while snails grew and most juveniles survived with access to radulated, fungi-rich leaves.
Silliman and Newall propose that this is "low-level farming," defined for fungus-growing animals as having adaptations for modifying local ecosystems to encourage or protect fungal growth, for providing a substrate to promote growth, and for consuming the cultivated fungus. There are many examples of comparable low-level farming among people.
Australian anthropologist Rhys Jones coined the term "firestick farming," which he first applied to the practice of Australian Aborigines' burning overgrown grasslands to encourage tender new leaves to sprout. The flush of green grass stimulates breeding in small marsupials that feed on it and attracts larger grazing marsupials such as kangaroos, creating a handy, well-stocked meat market for the pyro-agriculturalists.
Similarly, environmental historian William Cronon, in a 1983 book Changes in the Land: Indians, Colonists, and the Ecology of New England, described how Native Americans in New England burned the forest near their villages to create large sunny open areas under the trees that survived the blaze. Elk, deer, turkeys, and other game species flocked to these spaces to find food; moreover, plentiful nutritious food for the herbivores stimulated and enhanced their breeding and thus their abundance. The open habitat also provided favorable conditions for edible wild fruits such as raspberries and strawberries. As Cronon wrote, the Native Americans "...were not just taking the ‘unplanted bounties of nature'; in an important sense they were harvesting a foodstuff which they had consciously been instrumental in creating."
On the other hand, it is possible that the snails' apparent farming is just a byproduct of their feeding behavior, not an adaptation. African forest elephants, for instance, are sometimes called forest gardeners. Working in central Africa, conservationist Stephen Blake and his colleagues found that forest elephants "plant the forest on an elephantine scale with more than 100 species of seeds." The elephants eat fruit in one place and a few days later deposit the seeds in a nutritious mass of dung more than 35 miles away. Eventually some of these seeds will grow into trees from which the elephants can pluck tasty fruit. Although no other animals do this on quite the scale of forest elephants, many fruit- and seed-eating birds and mammals also "plant" their own food. Some squirrels, for example, bury acorns and influence the distribution of oaks in deciduous forests of the eastern U.S. In Arizona, mockingbirds, cardinals, and curve-billed thrashers eat chiltepines (wild chili peppers) and defecate the seeds under hackberries, ideal sites for germination and survival.
Bert Hälldobler and E.O. Wilson, in their massive 1990 book called simply The Ants, describe similar behavior among some ants. So-called harvesting ants, a variety of species that range from occasional seed-eaters to specialized granivores, gather seeds and store them in granary chambers within their underground nests. To prevent the seeds from sprouting, the ants nip off the growing tips before putting them in storage. But some seeds escape the ants' effort to kill them and manage to sprout, whereupon they become inedible to the ants. To clean the kitchen, the ants carry the sprouted seeds to the refuse heaps that edge or sometimes encircle the nest, giving the appearance that the ants are actually planting seeds for a future harvest. This behavior does, however, help to disperse the seeds of the plants the ants prey on, and may thus compensate the plants for their losses.
In all of these cases, it is unlikely that the animals' behavior is an adaptation for maintaining or increasing their food supply. Rather, it is simply the serendipitous result of their feeding ecology.
A perhaps analogous human activity, tossing leftovers onto the ground near one's home, has been suggested to have contributed to the domestication of some crops. This is called the dump-heap theory, and goes like this: Women, who likely were responsible for disposing of household waste, noticed food plants growing in the dump and began to more actively experiment with growing them. While experts agree that such a scenario is unlikely for the domestication of crops like wheat and other cereals, it may have played a role in that of fruit and root crops and some vegetables. And some scientists believe that fruit and root crops may have been cultivated before grain. Bruce D. Smith, of the Smithsonian's Museum of Natural History, is the world authority on the origins of domestication in the New World. He found that squash was domesticated in Mexico about 10,000 years ago, while maize came under human control at least 1,000 years later.
Herder Ants and Aphids
"The extreme myremecophilous [ant-loving] aphids
have evolved to the status of little more than domestic
cattle."
—E.O. Wilson, in Sociobiology (1975).
In addition to ant farmers, there are ant herders and nomadic pastoralists as well, with aphids playing the role that cattle and sheep do in human systems.
A variety of ant species rely for some or all of their sustenance on the excretions of aphids. Aphids feed on the sap of plants, and their sugary excretions are known as honeydew. Other insects in the same group, called Homoptera, excrete similar substances. The Biblical "manna from Heaven" was most likely the excretion of a scale insect, which is still sometimes collected in the Middle East.
Aphids that are not associated with ants either kick away the honeydew droplets with their hind legs or squirt the drops away as they emerge from the anus. Aphids attended by ants, however, defecate in such a way as to make it easy for the ants to lap up the honeydew. In some cases, the aphids have setae that form a basket around the anus to hold the honeydew until the ants eat. In other species, an aphid does not release the honeydew until stimulated by an ant fondling it with its antennae and forelegs. Other aphids appear to solicit ants by lifting their hind legs and exposing the anus when an ant is nearby.
So what's in it for the aphids? The ants provide them with a variety of services. They keep the aphids' neighborhood clean of sugary dung, which would likely attract other sugar-eaters. When the aphids are enclosed in an ant nest, they are protected from weather. And ants directly defend the aphids from predators, the aphids having lost their own defenses as domesticated animals often do. The ants' success in protecting their flocks is attested in the lengths that green lacewing larvae (Chrysopa glossonae) go to sneak past ant defenders to catch woolly alder aphids (Prociphilus tesselatus). Hälldobler and Wilson wrote, "The aphids derive their common name from filaments of waxy "wool" that cover their bodies. The [lacewing] larvae disguise themselves by "plucking" some of this material from the bodies of the aphids and applying it to their own backs. In other words, they employ the "wolf-in-sheep's–clothing" strategy to fool the ant shepherds that guard the aphids."
An extreme example cited in The Ants is that of the American corn-root aphid (Aphis maidiradicis) and an ant (Lasius neoniger). Colonies of this ant keep the aphids' eggs in their nests over the winter, and, when the eggs hatch into nymphs in the spring, carry them to the roots of the aphids' food plants. If the plants are uprooted, the ants retrieve the aphids and tote them to another food plant. The ants also repel potential predators and parasites from their aphid flocks and, similarly, the ants treat the aphid eggs as their own, by, for instance, carrying them to safety when the nest is disturbed. When the aphid nymphs turn into winged forms that disperse without the help of ants, they may be adopted by the ants that live in the aphids' new home.
Another is the nomadic herding behavior of a Malayan ant called Hypoclinea cuspidatus on which a mealy bug called Malaicoccus formicarii entirely depends. The mealy bugs live in the nests of the ants, called bivouacs, which are actually formed of the bodies of ants clinging to each other to form a blanket that covers the bugs as well as their own brood. For the mealy bugs to feed on sap of young plants, the ants carry the bugs in their mouth parts along a trail from the bivouac to a feeding site that may be more than 60 feet away. The ants stay with the bugs, harvesting their honeydew while the bugs suck in sap. If they are disturbed, the ants pick up the bugs, which raise up like a child raises its arms to get a lift from mom, and carry them away. When the young plants on a particular feeding site are spent, the ants gather up the mealy bugs, return them to the nest, and then quickly create a new trail to a new site. Then, when the feeding sites get too far flung, the ants pack up their bugs and their brood and migrate to greener pastures. The ants do no other hunting, and can't live without the bugs' honeydew, while the bugs can't make it without their ant caretakers, succumbing to starvation or predation by ants of other species.
Domesticator or Domesticated?
"[Wheat] now covers more than 600 million acres
of the surface of the planet. . . [People in the future]
will classify us, perhaps, as puny parasites, victims
of feeble self-delusion, whom wheat cleverly exploited
to spread itself around the world. Or else they will
see us in an almost symbiotic relationship with edible
grasses, as mutual parasites, dependent on each other
and colonizing the world together."
—Felipe Fernández-Armesto, in Near
a Thousand Tables: A History of Food (2002).
Only recently have scientists begun to wonder who has domesticated whom in human relationships with domestic animals and plants. Did people mold the ancestors of domestic cats, Felis sylvestris libyca, to suit their purposes, or did wild cats find tolerating people a small price to pay for the superabundant rats and mice that lived on human food and waste? This species certainly took advantage of people to move all over the globe and to achieve astonishing success: There are an estimated 70 million owned cats in the United States, a figure that doesn't include many million more feral cats. The relationships between people and domestic animals are likely far more complex than was once assumed.
Behavioral ecologist Mueller speculates that ant-fungi evolutionary relationships may be quite complex as well, asking whether, "attine fungiculture arose through a true domestication process serving the evolutionary interests of the ants or whether fungiculture may have arisen out of ancestral ant-fungus associations that originally served the evolutionary interests of the fungi." As mentioned above, the relationship may well have begun with a fungus making ants its dispersal agent. Mueller outlines several other areas in which the interests of ants and fungus might diverge, with the fungus potentially actively influencing the activities of the ants. For instance, fungi might produce chemicals that affect what plants the ants collect to feed their gardens. However, the view that ants are running the show has been so dominant that this research is just beginning.
Learning From Ants
"Perhaps, apart from providing us with a glimpse
at possible evolutionary outcomes of human agriculture
millions of years from now, the insect farmers can teach
us more imminently about epidemiological principles
and disease management of agricultural pathogens. After
all, they have been farmers for millions of years, and
maybe they have figured out a trick or two that leads
to their remarkable agricultural success."
—Mueller and Gerardo, in Proceedings of the
National Academy of Sciences (2002).
Natural systems are always changing. When it comes to something that reproduces as rapidly as fungi or bacteria, a system is never stable for long. Within a short amount of time, a generation of Escovopsis evolves to circumvent the antibiotics' ability to suppress it. And, as the presence of current-day attines can attest, the bacteria evolve and fight back. This is the "evolutionary arms race" that humans, who have been using antibiotics for only 60 years, are having trouble keeping up with. How is it, then, that these tiny creatures have been such successful users of antibiotics for 50 million years?
The attine system is "a perfect little model" and the "potential is there for a lot of useful information," Schultz remarks. "We need to understand what it is that the bacteria do to control the fungus—what substance it is producing." People mass produce chemicals that we find in nature and use them against a target like harmful microorganisms. However, the target evolves to evade chemicals, and becomes dangerous to humans once again. We then have to produce variants of those chemicals to fight the target effectively. "But, in the ants, you have a living system. It's a living culture of bacteria, and in ways we don't really understand, those cultures are being selected for their ability to control Escovopsis and the evolutionary response is immediate. ... I'd like to think humans would learn that instead of just inventing antibiotics. We run a somewhat more natural experiment, maybe engineer bacteria cultures with targets and target variants. It seems like a natural idea. We could just come up with models. Just think about the level of variation you could model inherent in a culture of bacteria versus a chemical you pretty much manufacture."
Understanding the biology of this bacterium could also help formulate a kind of control for pest populations of leaf-cutter ants. Leaf-cutter ant colonies in aggregate can weigh as much as an adult cow and daily displace as much fresh vegetation as one. In one year, a nest may consume over half a ton of leaves. Schultz labels leaf-cutters "the number one scourge in Neotropical agriculture" of Central and South America.
Leaf-cutters reach as far north as Texas and Louisiana, where they cause millions of dollars' worth of damage every year. They harvest agricultural products and compete with cattle for grass, collect dried foodstuffs such as grains, flour, and cattle meal, and have even caused the collapse of small buildings by undermining the foundations with their massive underground nests.
Controlling pest populations of leaf-cutters with insecticide is difficult due to the vastness of their nests and because attines eat only the fungi that they grow. But, there is potential for developing a control by disrupting the ant-bacteria symbiosis. By applying a bactericide that kills the actinomycete, breeding infected strains of bacteria, or even developing a strain of Escovopsis that is resistant to the actinomycete, the ants would be less capable of fighting off the pathogen fungus. The pathogen fungus would eventually destroy the ant gardens. However, Schultz cautions against the applied uses of such knowledge and warns of the dangers of affecting populations of lower attines or leaf-cutters that aren't in agricultural areas. The removal of these important soil-regenerating herbivores would have a devastating and destabilizing effect on the ecology of the area. Currently, the only serious threat to these animals is habitat destruction, for which people are responsible. Some ants destroy our farms and we destroy theirs.
Mueller and Nicole Gerardo wrote: "Like humans, the insect farmers became dependent on cultivated crops for food and developed task-partitioned societies cooperating in gigantic agricultural enterprises. Agricultural life ultimately enabled all of these insect farmers to rise to major ecological importance. Indeed, the fungus-growing termites of the Old World, the fungus-growing ants of the New World, and the cosmopolitan fungus-growing beetles are not only dominant players in natural ecosystems, but they are also major agricultural, forestry, and household pests."
It's not much of a stretch to make the latter two points about human farmers, too. They are certainly of major ecological importance and, arguably, from the perspective of natural ecosystems, major pests.
—Susan Lumpkin is the Editor of ZooGoer, and Stephanie Hsia is a former ZooGoer intern.
ZooGoer 33(4) 2004.
Copyright 2004 Friends of the National Zoo.
All rights reserved.
