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The First Farmers
by Susan Lumpkin and Stephanie Hsia When anthropologists look to the animal world for insights into human behavior, they usually focus on our closest relativeschimpanzees 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. In this Issue The First Farmers Farming, From Ancient to Zoo Trouble in Paradise: California's Island Fox Books, Naturally Current Issue Browse Archive About ZooGoer Advertising in ZooGoer Related Resources Kids' Farm at the National Zoo Leafcutters at the National Zoo Ant Agriculture at the Museum of Natural History Join FONZ to receive ZooGoer in your mailbox!
This Atta cephalotes is one type of leafcutter ant that grows crops of fungus in its nest. (Scott Bauer/USDA ARS)
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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 leafcutter 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 notshe 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 lifeas long as ten yearsdoing 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 workerssome 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 systemants 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 antibioticproducing 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 whichthe ants or the fungigot 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 mid1800s is a classic example. Proto-farming: Snails and Such Recently, another invertebrate has been added to the insectfarmer 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 organto 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 leavesand nearly half of all juveniles tested died on diets of uninjured leaveswhile 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 pyroagriculturalists.
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 herbivores the 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 curvebilled thrashers eat chiltepines (wild chili peppers) and defecate the seeds under hackberries, ideal sites for germination and survival. Bert Hlldobler 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 sugareaters. 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). Hlldobler 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-insheep'sclothing" 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 selfdelusion, 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 Fernndez-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...