Scientific American, March 2017
THERE IS, DESPITE THE NAME, NOTHING URBAN ABOUT PIPER CITY, ILL. It is a farm town with a skyline of grain elevators, a tidy grid of pitch-roofed houses and, a few blocks beyond, endless fields: corn, soybean, corn, soybean, corn, corn, corn, perfectly level, perfectly square, no trees, no cows, no hedgerows, no bare land. In late August of 2013, a man named Joseph Spencer followed a corn-flanked county road northwest from Piper City until his GPS advised him to leave the road altogether and turn onto a gravel track. Spencer, an entomologist who studies farm insects, was looking for a farmer named Scott Wyllie.
In good growing years, crop corn around Piper City and elsewhere is as standardized and predictable as a widget rolling off an assembly line: the plants have the same spacing, the same height. Wyllie’s corn, however, had developed a personality. The stalks had twisted back on themselves like the neck of a goose. Spencer could pull one from the ground with a flick of his wrist; the once white roots underneath were gnawed and brown, like teeth gone rotten. Some plants had tipped over from their own weight. And the air was teeming with grain-sized, yellow-and-black striped beetles. They clambered on leaves, mating, defecating and munching on corn silk. Spencer had to close his mouth to keep the insects out. The beetles are Western corn rootworms, and it had been their wormlike larvae that gnawed Wyllie’s corn roots to destruction. Wyllie, who farms 1,000 acres, told Spencer he had done everything the experts recommended to fight the insects. He rotated his corn crop with soy every other year to interrupt the rootworm food supply. He planted corn seeds that were genetically engineered to release a toxic protein that kills the hungry larvae. But in the field that day, Spencer could see that these approaches—the most successful and widely used strategies to fight the pest—had failed. “I got a chill down my back,” Spencer remembers. “I thought, ‘This is it. The worst-case scenario.’” Spencer has spent most of his career studying rootworm behavior at the Illinois Natural History Survey at the University of Illinois at Urbana-Champaign. And he knew that the insects swirling around him meant trouble not only for Wyllie’s crop but for the entire Midwestern corn belt.
The rootworm— Diabrotica virgifera virgifera —is the most expensive and consequential pest in American agriculture. It is known as the “billion-dollar bug”—although in fact it probably costs the U.S. closer to $2 billion every year. The beetle spends its life cycle on corn, and corn is the nation’s largest crop by far. It frequently covers 80 million acres and sometimes more. The crop brings in $50 billion in annual sales. Farmers spend hundreds of millions in chemicals, seeds and labor fighting it. Agriculture companies spend hundreds of millions developing products to help them do so.
The result is an evolutionary arms race: the beetle damages farmers’ crops; seed companies create a product to kill it; the beetle evolves to resist the product; the corn gets infested again. And then, “just in time, the good guys in the white hats ride into town,” Spencer says, with a new beetle-killing weapon. For the past decade the weapon of choice has been famously controversial genetically modified corn plants that make chemicals to kill rootworm larvae. But Spencer saw in Wyllie’s fields that rootworms were winning.
Today farmers and scientists are pinning their hopes on a new modification—a corn laced with special genetic molecules that work within a rootworm cell nucleus to shut down crucial genes. The new technology should arrive in fields by the end of this decade. But environmentalists are concerned gene alterations may harm helpful insects such as ladybugs. And scientists and farmers alike know it is only a matter of time until the rootworm evolves to resist the new corn. “You can’t stop resistance,” Spencer says. “You can only slow it down.”
BEHAVIOR CHANGE
Spencer’s office at the Illinois Natural History Survey is littered with corn paraphernalia: corn-themed signs, mugs, bottles and silverware he picked up from eBay. His colleagues there call him “Cornboy,” and although Spencer turned 53 last October, there is indeed something boyish about him, from his Dennis the Menace grin to his impish enthusiasm for all things corn and rootworm. (Draped over his desk chair is a T-shirt he made: two mating rootworms and the caption, “We like to watch.”)
His calling was born of calamity. In 1987 an entomologist with the Natural History Survey named Eli Levine got a call from a Piper City grain-elevator agronomist who was seeing damage in corn that had been rotated with soy. Scientists believed this to be impossible. Because Western corn rootworms feed exclusively on corn and lay their eggs there, farmers had been able to control the beetles simply by swapping corn and soy fields every year—when the larvae emerged in soy the next spring, there was nothing for them to eat. Levine drove out to Piper City to look for another explanation. There wasn’t one. “The beetles were laying eggs in soy,” he says.
This wasn’t the first time the rootworm had changed its behavior. When entomologist John Lawrence LeConte first wrote about the beetle in Kansas in 1868, it was a harmless chewing insect from Central America found in low populations on the Western Great Plains. The adults emerged from the ground in early summer, fed on maize, squash and prairie grasses, mated, laid eggs in crevices in the soil, and died before the first frost. In the spring, the eggs hatched into tiny, white, maggotlike larvae, feeding underground on roots until it was time to emerge. It was only with the advent of efficient center-pivot irrigation in the 1950s, which allowed continuous mass production of corn, that rootworms spread east from Colorado and Kansas across prairie lands that had been converted to cornfields. By 1964, when the beetles arrived in Illinois, they were already resistant to many of the insecticides farmers used to fend them off. And sometime before Levine visited Piper City, some mutant females did something they had never done before: a restless few flew into a field of soy and found that their guts could tolerate soybean foliage long enough to lay eggs there. The next year their progeny emerged to a feast of corn. It was an immensely advantageous adaptation. The beetles had found a way to resist not only modern pesticides but also modern farming practices.
In 1996, after growers in Illinois and Indiana suffered massive losses to these new rootworms—the infestation was so bad that window washers on Chicago’s Sears Tower reported masses of wind-borne beetles mobbing their platforms—the survey hired Spencer to study the rootworm’s troubling new behavior. Spencer had done his graduate work on onion flies, and his talks on the obscure insects attracted only a couple of hundred people, max. When he gave his first lecture on rootworms, however, more than 1,500 farmers and researchers attended. The crowd was dead-silent, rapt. “I thought, ‘Wow, this is a cool insect. People care about it,’ ” he says.
TARGETED INSECTICIDE
As resistant beetles continued to spread from Illinois to Iowa, Michigan, Missouri, Ohio, Ontario and Wisconsin, farmers found themselves in a bind. Their livelihoods depended on healthy corn, and they felt they had little choice but to douse acre after acre of their seeds with high levels of toxic, broad-spectrum insecticides. Nobody—not farmers, not entomologists, and especially not the Environmental Protection Agency—was happy about it.
Which is why, in 2003, when the agribusiness behemoth Monsanto came out with a hybrid corn engineered to produce a protein that killed rootworms, farmers rushed to get it into their fields. The company (which funds some of Spencer’s research) had already produced a hybrid corn plant with an added gene from a soil bacterium, Bacillus thuringiensis (Bt), that was toxic to a moth called the European corn borer. The product proved remarkably effective: there are so few corn borers now, Spencer says, that his current graduate student has never seen the moths outside of a laboratory. Monsanto used a different strain of Bt to engineer the new anti-rootworm toxin, called Cry3Bb1, which bound to the guts of rootworm larvae, creating holes in the worms’ digestive lining and killing them.
For about five years farmers who planted the new rootworm-killing seed achieved the same happy results they had seen with the corn borer. But in 2009 Iowa farmers began seeing damage again, and it soon became clear that some rootworm populations had developed resistance. The beetles in Wyllie’s field, in fact, proved impervious to crop rotation and to at least two types of Bt toxins. They were, Spencer says, “the baddest rootworms around.” Last summer scientists documented resistance to a third toxin; a fourth one has held up in the field, but lab tests indicate that some populations are growing less susceptible to that toxin as well.
Because resistance appears inevitable, Spencer is taking a closer look at rootworm behavior, hoping to figure out which rootworms are most likely to move around and spread troublesome traits—not all the insects disperse equally. It is possible that knowledge could help contain the pests, he says, by helping the ag companies design and deploy the “next best thing in a way that matches the reality of what the insects are capable of.”
On a humid afternoon last July, he and a team of student helpers head out to the Lost 40, a test plot located near the Natural History Survey labs, where four yellow, 30-foot scaffolds loom over the fields. Spencer grabs a bug net and a cooler full of vials and dry ice, hooks them to a carabiner and climbs a scaffold. “Up we go!” he says, “to get the best view in Illinois!” Three helpers head up the three other platforms—two in corn and another that towers above a crosshatched corduroy of soy. Other students move to spots on the ground in strips between fields. “Everybody turn on their walkie,” Spencer says. He’s the geek explorer: Tilley hat, khaki bandanna, zip-off pants, stopwatch, reading glasses, multiple pens in his pocket. He waves his net high in the air. “In 40 seconds we’re going to start the 6:17 collection,” he announces.
The team plans to conduct eight collection periods of 10 minutes apiece, during which they will catch as many rootworms as possible. By doing so, Spencer hopes to better understand “the populations that leave and the ones that don’t”—and whether beetles that resist Bt corn and crop rotation are more likely to leave their home fields. Some rootworms are talented long-distance travelers. Once the insects rise above the layer of turbulent air below the scaffolds, he says, “they’re going to go a long way.” They can relocate as far as 100 miles if caught in the convective updrafts of thunderstorms. Spencer has old photographs of billions of rootworms piled two to three inches deep along the shore of Lake Michigan after one such storm.
From above, the corn looks like a very large marching band, tasseled hats crowded impossibly close—“the massed multitudes,” Spencer says. When he first arrived in Illinois, he sometimes caught up to 15 beetles a minute. “It snowed rootworms.” But beetle populations have been low in the post-Bt years, and floods in the spring of 2015, which drowned many larvae in the ground, suppressed populations even further. That summer he caught nine beetles all season. He calculates that the effort cost his lab about $89,400 per rootworm ounce, with labor and material costs. That is more than 80 times the price of gold. (Now every spring he offers his students a prize: 10 gold dollars if they catch the first adult rootworm of the season. Then Spencer eats the insect. “They’re not delicious or anything,” he says. The wing casings get caught in his teeth.)
The sun drops lower over the jungle of corn. Spencer sees something off in the middle distance. He races across the scaffold, leans far out over the guard rail, and swishes his net up and out. “Woohoo! I caught a rootworm!” He examines the beetle deep in the net—“My heart’s racing!”—then opens the cooler and flash-freezes it—“Put her in a vial, blink! Awesome.” It is one of nine beetles the team will catch that night.
The next day he and his team dissect the insects in the lab, grinding each one into a vial of “beetle gemish” and testing their gut contents. The fields around the scaffolds are planted with two types of corn, each engineered with a different Bt trait. Dipping gene check sticks—they look like pregnancy tests—in the bug smoothie, Spencer “interrogates the beetles’ digestive systems” to determine which proteins are in their guts and thus where the beetles fed during the previous 24 hours. If an insect tests positive for a trait not present in his own fields or for two different traits, he knows that beetle is a “mover.” The team also sets up tents within cornfields, slurping the beetles up with “bugsuckers,” modified shop vacuums that look like Ghostbusters proton packs. If those beetles come from fields planted with rootworm-killing Bt, he knows they have developed resistance.
Spencer puts on magnifying “nerd goggles” and places a larva under a microscope—it’s a tiny, groping “neonate,” between two and three millimeters long, white and newly hatched. It is in this life stage that the rootworm finds the corn roots on which it does much of its billion-dollar damage. “This little thing,” he says, “is the worm that roars.” Next he places six yellow-andblack adults under the microscope; they run up and down the sides of their clear-plastic cage. One mated female camps herself in a corner with a corn silk. In an instant, she gobbles the filaments down to nothing. Her swollen, oily abdomen wiggles as she eats, and a froth spreads across her face. It is almost, I dare say, cute. But her hunger—her desperate evolutionary drive to survive and reproduce—is anything but.
A GENETIC ATTACK
The ag companies haven’t, of course, given up on taming that hunger. Monsanto, DuPont Pioneer, Syngenta and Dow Agro-Sciences all sell engineered seeds that kill rootworms, and they, too, have evolved in the face of growing insect resistance to their products. In 2009 they began to combine different Bt toxins for rootworms into one corn plant. These “stacked” products offer a more effective strategy for delaying resistance, working from different angles much as a multidrug “cocktail” does to control HIV in humans. After Wyllie’s bad summer in 2013, he switched to a stacked Bt corn, and his beetles are now under control. But with three of the four traits on the market failing, there may not be anything to stack in coming years. “If you have a trait that’s already compromised and you combine it with another trait that’s working well,” Spencer says, “it’s functionally acting like a single-drug cocktail,” rendering the good trait more vulnerable to resistance without the protection of a second effective trait. Farmers need new ingredients to add to the cocktail. Researchers at DuPont Pioneer recently announced the discovery of a new bacterial gene that kills rootworms, but because it takes about 12 years and $136 million to shepherd a new GM trait through the regulatory process, it will not be available to farmers any time soon.
There is one new ingredient that may join the cocktail sooner, however. Monsanto is seeking regulatory approval for a corn seed that would integrate two older Bt toxins with a new technology called RNA interference, or RNAi. The technology uses targeted RNA—the ubiquitous molecule that transmits genetic code and helps to assemble proteins—to turn off or turn down specific genes. When rootworm larvae eat the corn, segments of double-stranded RNA, created in a lab and incorporated into the plant, bind to and interfere with an insect gene that produces proteins essential to waste storage and disposal within the rootworms’ cells. Without those proteins, the insects die.
The RNAi trait has received initial regulatory approval from the U.S. Department of Agriculture and the Environmental Protection Agency, and Monsanto hopes that the final Bt-RNAi corn seed will win epa approval by the end of this decade. If it does, it would be the first wide-scale application of RNA interference in corn agriculture. (Monsanto currently has an experimental-use permit to test the product on outdoor plots.)
It is a promising technology. Traditional pesticides function much like incendiary bombs, destroying intended targets, such as rootworms, but creating vast collateral damage among beneficial insects, aquatic species, birds and mammals. RNAi works, instead, like a ninja, using unique sequences of synthetic genetic code to take out only its intended victim, then disappearing (RNA degrades quickly in the environment). “It’s the ideal pesticide,” says Stephen Levine, a toxicologist at Monsanto. “It’s specific. It does what it’s supposed to do. Then it goes away.”
That is the theory, anyway. In a 2012 paper, however, a Chinese research team reported that it found snippets of RNA from food plants in the livers of mice that consumed those plants. The RNA affected a cholesterol-regulating gene also found in humans. This “cross-kingdom effect” was surprising because these types of RNA were not thought to survive in the hostile environment of the mammalian gut; if true, the results raised the possibility that RNAi in plants could affect humans. A study presented at a conference in 2013 found that RNA created to kill rootworms could also kill ladybugs, a beloved beneficial insect. That same year Jonathan Lundgren, an entomologist then at the usda’s North Central Agricultural Research Laboratory in Brookings, S.D., published a paper suggesting that RNAi could affect nontarget organisms in unexpected ways. He also says the USDA hindered the publication of another paper he wrote about RNAi and honeybee genomes. Lundgren has since resigned and filed a federal whistle-blower suit. “I’m not against RNAi,” he says, “but the potential exposure of a corn product is so large.”
RNAi is the perfect example, says Martha Crouch of the Center for Food Safety, of the “chaos of an emerging technology” that seems to promise only progress, until “the oops moment when something unexpected and harmful” happens—such as ozone holes, carcinogenic children’s pajamas, rat-sized-rootworms. “There are,” Lundgren adds, “too many knowledge gaps.”
But many scientists think there is ample evidence of safety. Despite efforts to do so, other researchers have been unable to reproduce the rodent findings. In considering approval of Monsanto’s RNAi-engineered corn plant, an EPA panel concluded that “there is no convincing evidence” that double-stranded RNA is absorbed in the guts of humans or other mammals in a form that causes harm. “What are the chances that it will affect humans? Essentially zero,” says Craig Mello, a molecular biologist at the University of Massachusetts Medical School who co-discovered RNAi in 1998 and won a Nobel Prize for that discovery in 2006. RNAi is very organism-specific, adds Monsanto toxicologist Pamela Bachman. Rootworms do share some gene sequences with other insects, including the one that killed ladybugs in the 2013 study. But Monsanto’s product targets a sequence that is not shared with ladybugs or other beneficial insects found near cornfields. “Sequence matters,” she says.
CONTAINMENT
At David Masching’s 2,300-acre farm outside Piper City, Spencer meets with a group of corn growers, Wyllie among them. They sit around a table in a barn that looks more like a hangar, with soaring ceilings to accommodate Masching’s impressive collection of farm machines.
The growers wear ball caps, work boots, T-shirts. None farm fewer than 1,000 acres, and all work their land alone, with some family and seasonal help. Even so, margins are slim. When corn prices approached $7 per bushel in 2012, a northern Illinois corn farmer could clear more than $300 per acre after paying for seed, fertilizer, fuel, rent and crop treatments. But corn prices plunged in 2015, and growers lost $65 for each acre they planted. “You can understand,” says Spencer’s retired colleague Michael Gray, who joined Spencer in Masching’s barn, “why producers don’t take a chance with rootworms.”
Nor other organisms, for that matter. On the way to Piper City, Spencer points out a crop-dusting plane, laden with a “tank mix” of wide-ranging fungicides and pyrethroid insecticides, swooping and angling above the fields. In cornfields worked by most Illinois farmers, you are not likely to see bugs. “It’s disconcerting for an entomologist to go into a cornfield and not see an insect,” Spencer says. “The ground is sterile. That’s what farmers want.”
Farmers want security, whether delivered by engineered seeds or dropped from the sky by crop dusters—even if this “insurance mindset,” as Spencer describes it, speeds up the treadmill of chemicals and resistance. Farmers want predictability. Where growers once rotated corn, wheat, alfalfa, sorghum and oats, it is now corn and soy and corn and soy again. The rootworm thrives on predictability. Monoculture makes it easy for a lone grower to farm 2,000 acres. But it also makes it easy for the rootworm to destroy those acres. “We created this pest,” Gray says. “We gave it a wonderful life,” Spencer adds.
Life has been less wonderful for the rootworm in Europe, where the insect turned up in the early 1990s; it seems to have hitched a plane ride from Chicago to Serbia and spread from there. The beetle’s trans-Atlantic journey prompted European farmers to fear the same levels of devastation seen in the U.S. But Europe has smaller farms, whose operators plant less corn and rotate it with a wider variety of plants. The insect does some damage in regions where farmers plant corn continuously, but overall populations remain under control. “The rootworm is not a problem in Europe,” says researcher Stefan Vidal of the University of Göttingen in Germany, who helped to coordinate the European Union–funded response to the rootworm invasion. Diversity, European farmers concluded, is the best defense.
In the American corn belt, farmers do not feel they have that option. They are too big to fail, yoked to horizon-to-horizon economies of scale and the technological investments that enable them to make a living in America’s hyperspecialized commodity market: the $400,000 combines, the hangar-sized barns, the pesticides, engineered seeds and the double-stranded RNA. It has become an escalating arsenal of silver bullets that inevitably miss their shifting mark.
Rootworms have brains so small that you can barely dissect them. But evolution has its own intelligence. “It’s a lesson that we have failed to learn over and over and over,” Spencer says. “Natural selection is always going to win.”