Danielle Gerhard, PhD,Wed Jun 11,
In the fall of 1917, on a cotton farm in Hearne, Texas, entomologist Ivan Shiller documented the first pink bollworm sighting in the US. The insect, named for the characteristic pink color it develops during its larval stage, is one of the most destructive cotton pests in the world. “The pest lays its eggs in cotton bolls, where they hatch into ravenous larvae that gorge on cotton seeds and strands,” said Eoin Davis, an assistant director at the Animal and Plant Health Inspection Service (APHIS), an agency of the US Department of Agriculture (USDA).
In 1917, Ivan Shiller found the first pink bollworm in the United States in Hearne, TX.
USDA Pink Bollworm Project Photograph Collection
After two weeks of feasting, the larva exits the boll and drops to the ground, where it spins a cocoon and pupates. From this cocoon emerges a grayish-brown moth, ready to mate and begin the pink bollworm life cycle anew.
The pink bollworm is an incredibly successful pest. As many as six generations of pink bollworm can occur per year, and a single female moth can lay anywhere from 100 to 200 eggs on a boll. By burrowing into the bolls, the pink bollworm larvae are protected from pesticide sprays and predators, complicating pest management efforts. Larvae that are present at the end of the growing season go dormant in winter and reemerge in the spring to restart the cycle of life. “It’s such a difficult animal to control,” said Peter Ellsworth, an entomologist at The University of Arizona.
By 1965, the pest had established itself across the southwest states of New Mexico, Arizona, and California where it would go on to destroy acres of crops and cause economic hardship for farmers for decades. “By 2000, the pink bollworm was costing growers in these states about $32 million annually in management costs and yield losses,” said Davis.
The caterpillar of the pink bollworm destroys cotton yield by devouring the seeds inside cotton bolls. Organisms that cause boll rot can enter the holes created by the pink bollworm larvae. Peter Ellsworth/The University of Arizona For decades, farmers, researchers, and industry leaders coordinated efforts to suppress pink bollworm populations across the nation’s cotton-growing regions. But around the turn of the century, a bold new idea took hold—one that shifted the goal from controlling the pest to wiping it out entirely.
Sterility, Sprays, and Scents, but the Pink Bollworm Persists
The pink bollworm, which is native to Asia, is thought to have hitched a ride into the US via seeds coming from Mexico, and into Mexico via seeds imported from Egypt around 1911.1 The US government recognized the threat that the pink bollworm posed to the nation’s cotton industry early on, and in 1918, they established a pink bollworm research facility in Lerdo, Durango, Mexico. Over the following decades, sub-laboratories sprang up across the Southwest of the US to study the pest’s biology and behavior, which in turn shaped management strategies. These included scheduled insecticide applications to kill as many adult moths as possible, quarantines on cotton from infested areas, delayed planting dates to trigger suicidal emergence of overwintering larvae, and stalk-destruction deadlines to reduce the starter population for the following season.
Although these cultural control tactics helped slow the spread of the pink bollworm across Texas, progress hit a roadblock. Heavy rains during the fall of 1951 delayed the cotton harvest and stalk-destruction, and many rain-damaged crops were left in the fields. Consequently, pink bollworm populations exploded in 1952, causing devastating crop losses across the state. This led USDA researchers, cotton growers, and the National Cotton Council to join forces, forming the Pink Bollworm Advisory Committee and the Pink Bollworm Technical Research Committee, to ensure the coordination of research and control efforts across the state. There was no room for laxity in pest management.
Peter Ellsworth (right) worked closely with Steve Naranjo (left; now retired from the USDA) to research the pink bollworm and other cotton pests. Here they are pictured in a cotton field in Arizona in front of a USDA facility (on the left) and the University of Arizona Maricopa Agricultural Center (on the right).
USDA
The committees needed new tactics if they were going to halt the pink bollworm’s advances across the Southwest. It was around this time that USDA entomologists Edward Knipling and Raymond Bushland developed the sterile insect technique, a biological control method wherein sterile insects were bred and released into pest-infested areas at scale. The idea was that sterile insects would compete with their fertile counterparts for mates, but because they could not produce offspring, the next generation’s population would plummet. Radiation was a common sterilization procedure, but as Bruce Tabashnik, an entomologist at The University of Arizona, noted, “It’s a Goldilocks thing; you want just the right amount of radiation.” There needed to be enough radiation to sterilize the males, but not so much that it interfered with their ability to mate.
In 1968, the USDA, industry, and state agencies initiated a sterile pink bollworm moth release program in the San Joaquin Valley, a relatively isolated cotton growing region in central California that had never experienced a continuous pink bollworm population.2 They wanted to determine whether daily in-season sterile moth releases could help prevent the establishment of the cotton pest. The program lasted 24 years, and in that time, they made significant improvements to the sterile moth technology, including increasing their annual numbers and the mating propensity of the sterile males with wild females. In all those years, the valley never experienced a permanent pink bollworm population. Although promising, it was ultimately in a region without an active infestation.
Cotton fields in the south of the state and across the irrigated desert areas of the Southwest were not as lucky. Traps baited with sex pheromones enticed wild male moths, but the tactic was never successful enough to make much of a dent in the pink bollworm population. This left insecticide spraying—lots of it—as the main pest control approach. Because the chemical insecticides could not reach the larvae nestled inside the bolls, the goal was to kill as many adults as possible, which required regular spraying. Still, the pink bollworm persisted. “Not only was pink bollworm spraying not very efficient, but it was hazardous,” said Ellsworth. Beyond environment and human health concerns, regular and heavy insecticide use also interfered with growers’ ability to manage other pests.
Reflecting on the late 21st century, Ellsworth said, “It was a very difficult time, and it was existential in dimension, meaning, if we did not come up with a better solution soon, it placed the entire industry in jeopardy.”
Genetic Engineering Defeats the Pink Bollworm
Sticky pheromone traps placed throughout cotton fields were used to attract male pink bollworm moths and disrupt mating.
Peter Ellsworth/The University of Arizona
In 1902, a Japanese scientist isolated a bacterium from silkworm larvae suffering from an outbreak of “flacherie,” an often fatal disease triggered by ingesting contaminated mulberry leaves.3 Nearly a decade later, a German scientist identified the same bacterium in a diseased flour moth larva and named it Bacillus thuringiensis (Bt). The common soil-dwelling bacterium quickly drew
scientific interest due to its potent insecticidal effects coupled with its apparent safety profile for humans. Although Bt made its way into commercial insecticidal products as early as the 1930s, it wasn’t until the latter half of the century that researchers pinpointed its insect-killing power: During a process called sporulation, the bacterium produces crystals containing proteins—Cry for short—that are toxic to certain insects.
The genetic engineering boom in the 1980s drew interest from agricultural companies looking to solve long-standing problems in the field.4 Researchers began splicing cry genes into crops, enabling the plants to produce their own insecticidal proteins. One of these proteins, Cry1Ac, proved particularly effective against lepidopterans like the pink bollworm, and the gene encoding it became the primary cry gene used to create Bt cotton.
After screening hundreds of transformed cotton plants, one cotton line demonstrated consistent floral protection, good production of Cry1Ac, and outstanding insect control. Ellsworth recalls seeing aerial photos from some of the testing fields that showed an island of green Bt cotton plants surrounded by wild cotton that had been completely stripped. “It was really quite astonishing,” he noted. “It didn’t take too long to realize that Bt cotton was going to be an incredibly powerful weapon against pink bollworm.”
Finally, in 1995, the Environmental Protection Agency (EPA) approved the first Bt cotton variety for commercial use, which growers planted on 12 percent of the US cotton acreage the following year.4 “It was really a dramatic change for us, and it immediately reduced the use of many of these broad-spectrum insecticides, including some that were quite hazardous,” said Ellsworth.
Bruce Tabashnik, an entomologist at the University of Arizona, studies the evolution and management of insect resistance to genetically engineered crops, including Bt cotton. Alexander Yelich
The uptake of Bt cotton was swift. “There wasn’t a grower that was growing cotton in 1996 that didn’t recognize pink bollworm as one of their biggest challenges in production,” said Ellsworth. By 1997, the engineered crop comprised more than 60 percent of cotton acreage in the state.5
But this didn’t mean that moths went away. In fact, farmers were still required to plant a small percentage of non-Bt cotton on the fields, and this had to do with managing resistance. Tabashnik said that one of the misconceptions people had for decades was that insects did not develop resistance to Bt. But in 1990, Tabashnik and his team overturned the prevailing assumption when they reported the first field case of Bt resistance in the Diamondback moth in Hawaii.6
“In the United States, the Environmental Protection Agency was doing a balancing act,” said Tabashnik. They knew that advancing this technology would have massive implications for reducing the need for broadly toxic pesticides, but they also recognized the potential for resistance to quickly evolve. The solution? Structured refuges for the pink bollworm. Planting just a small acreage of non-Bt cotton alongside the Bt cotton ensured that there were always sources of moths carrying Bt
susceptible genes.
Planting structured refuges became the law of the land. “The growers here are very smart and very progressive and proactive,” said Tabashnik. “They understood that if they just planted Bt cotton and didn’t do something to slow the resistance, they’d probably get resistance, so they were all on board.”
Tabashnik’s team showed that only a tiny percentage of pink bollworm larvae survived on Bt cotton and that inheritance of resistance to the engineered crop was recessive.7 “The success of refuges is a numbers game,” he noted. To illustrate, he offered an example: Early field data showed that pink bollworm caterpillars were about 1,000 times more likely to develop and emerge from conventional cotton bolls than from Bt cotton. Based on this, if 50 percent of cotton was planted as refuges and the other half as Bt cotton, researchers could expect a 1,000-to-one ratio of moths from refuges per potentially resistant moth from Bt cotton. The actual planting percentages in Arizona from 1997 to 2005 were 37 percent refuges and 63 percent Bt cotton, which translated to about 600 moths from refuges per moth from Bt cotton.8 “With recessive inheritance of resistance and the low frequency of resistant moths, nearly all resistant moths are likely to mate with susceptible moths and produce susceptible offspring that are killed by Bt cotton,” said Tabashnik.
Mathematical simulations of responses to insecticides first suggested that refuges could slow the evolution of resistance, and evidence from the field supports these predictions for Bt crops.9,10 “Especially when inheritance of resistance is recessive, refuges work really well,” said Tabashnik. Consistent with predictions from models, the abundance of refuges and field outcomes varied dramatically among countries where Bt cotton targeted the pink bollworm, which can be viewed as a natural experiment.11 “The most striking contrast is between the US and India, where refuges were not planted and pink bollworm evolved resistance to Bt cotton very quickly,” said Tabashnik. Although there are a lot of other differences between the US and India that could have altered the outcomes, Tabashnik suspects the lack of refuge mandate enforcement that resulted in many farmers not following it to be a major contributor.
Although the refuge strategy was successful in delaying resistance to Bt cotton, planting non-Bt cotton meant that growers were purposely producing pink bollworm, making eradication impossible. Robert Staten, who had worked for decades on controlling pink bollworm with mass releases of sterile moths and applying female sex pheromone for mating disruption, championed the concept of using these tactics together with Bt cotton to achieve eradication. He retired in 2006 from his position as director of the USDA-APHIS program in Phoenix, then worked as a consultant with the National Cotton Council’s Pink Bollworm Action Committee to develop the plan for eradicating this pest from the cotton-growing areas of the US and northern Mexico.12 “Instead of growing refuges, which was the EPA-mandated policy at the time, the idea was that we’ve got the pink bollworm down—we’ve got our foot on its throat—let’s finish it off once and for all,” said Tabashnik.
An Integrated Pest Management Approach Against the Pink Bollworm Leads to Eradication
Removing the refuges entirely seemed risky to Tabashnik, based on his evolutionary biology training and research on insecticide resistance. “My bias was that insects will evolve resistance to anything, so the concept that we’re going to eradicate them, somehow that was totally against all that I believed in.” He started to get nervous. He wrestled with how to warn the farmers and Staten about the risks without overstepping. “My stomach was doing somersaults and heartburn and all that,” said Tabashnik. But then, the committee provided Tabashnik with a golden opportunity.
They wanted to replace the refuges with sterile moth releases and 100 percent Bt cotton fields. Knowing that Tabashnik had developed computer models to simulate resistance evolution under different management strategies, the growers asked him to model their plan. Tabashnik saw this as his lucky break—he could use the simulation results to show why their strategy wouldn’t work. Together with a postdoctoral researcher, he built a detailed model and plugged in the proposed plans. “No matter how we tweaked it, as long as we were somewhat realistic, we couldn’t get it to fail,” said Tabashnik.
Measures That Saved Cotton From the Pink Bollworm
After a century of wreaking havoc on cotton crops in the US, the pink bollworm was declared eradicated in 2018. This milestone resulted from a decade-long, highly coordinated integrated pest management program.
1) Billions of sterile male moths were released over cotton fields to vastly outnumber wild moths, including any that had developed resistance to genetically-modified cotton.
2) Traps, pheromone sprays to disrupt mating, and targeted insecticides offered additional layers of protection.
4) Cultural control practices, such as setting planting, harvesting, and stalk destruction dates to create a host-free period over winter, helped break the pest’s life cycle.
Like the refuges, it was a numbers game. As long as there were enough sterile moths, they could not only outnumber any Bt-resistant moths but also cause population collapse. He added, “I was like, ‘Okay, I’m a scientist. It doesn’t matter what I believed before I saw the results from the simulations,’” said Tabashnik. He got onboard. Soon thereafter, the EPA gave them the green light to go ahead with the integrated pest management program in cotton growing areas of the US, which included Texas, New Mexico, Arizona, and California.
“The amount of steriles they wanted to release was just incredibly huge,” said Tabashnik. In the end, the USDA released more than 11 billion sterile moths between 2006 and 2014 in Arizona alone.13 For this they would need a mass rearing facility.
Davis said that the farmers were essential to eradicating the pink bollworm, and they even helped foot the bill, covering about 80 percent of the costs of the eradication program. “In California, farmers even pooled their money to purchase a rearing facility in Phoenix, where USDA began producing the sterile bollworm moths for release. USDA provided the remaining 20 percent of the funding to help run the program,” said Davis, who was the director of the USDA-APHIS Phoenix Rearing Facility during the time of eradication program.
Years of research went into refining the mass rearing and sterilization process. “The technical and logistical challenges of insect production, sterilization, and distribution on this scale were enormous,” said Davis. “Even a slight tweak in one of the ingredients in the insect’s diet, for example, could alter production results.” They also had to optimize and coordinate large-scale releases of the sterile moths. “Small planes had to be retrofitted for our use and had to fly slowly and at very low altitudes to release moths without damaging them,” said Davis.
During the eradication program, more than 11 billion sterile moths were released by airplanes to overwhelm wild populations in the field. To generate the sterile moths, pink bollworm caterpillars were mass reared in a facility.
Alexander Yelich
It was no small feat to drop millions of sterile moths over fields all across the state in a coordinated fashion. “What these guys pulled off—it’s just incredible,” said Tabashnik.
The results on the integrated pest management program were almost immediate.13 The results of prior to 2006, the first year of the sterile moth releases, the cotton industry had seen a gradual reduction in pink bollworms thanks to the Bt cotton. However, in 2005, there were still more than two billion pink bollworms in Arizona. A year later, Tabashnik said that the number of pink bollworms dropped like a stone. “Before you know it, you’re not outnumbering just 200 to one, you’re outnumbering them 1,000, 10,000, [even] 100,000 to one, and that’s why the population crashes,” said Tabashnik. He added, “By 2010, the program, which was doing massive sampling, couldn’t find a single pink bollworm larva in the state of Arizona.” By 2013, APHIS and their partners did not trap any wild pink bollworm moths.
It wasn’t until 2018 that the USDA officially declared the pink bollworm eradicated from US cotton-growing regions. Although surveys and trap checks hadn’t detected a single larva or wild moth in years, the process of declaring eradication is deliberately cautious. The standard required five consecutive years with no pink bollworms in cotton bolls and no adult moths in traps. Before the program began, Tabashnik admitted he never thought they’d meet such a stringent benchmark.
“Eradication of an established pest is rare and hard to accomplish,” said Davis. “The pink bollworm program was successful because we created the tools we needed to succeed, and everyone worked together to leverage every tool at the right time.” While the sterile moth releases and Bt cotton were critical, other tactics also contributed to the successful eradication, including the use of female sex pheromone to disrupt mating and cultural control tactics, like imposing planting and harvest dates to create a host-free period over winter.
Although the pink bollworm was declared eradicated in 2018, intensive monitoring and management continue and also serve as an early-warning system in case the pest resurfaces. “Vigilance remains important,” said Ellsworth.
While Ellsworth said that the growers made this happen, he emphasized the importance of the science that enabled it. “There were many experiments, trials, false starts. There was animosity. There were people absolutely against the idea of an eradication program–growers even. There was politics. There was money. But in the end, there had to be a lot of science to support the successful deployment of this program.”
“The public good that’s been had is extraordinary,” said Ellsworth. “We’ve created an extraordinary [integrated pest management] outcome that is safe to the environment and to the people that live and work around these agricultural areas and preserved a crop and a culture and a rural economy that may have disappeared otherwise.” (Source: www.the-scientist.com)