Transgenic cotton and sterile insect releases synergize eradication of pink bollworm a century after it invaded the United States.

Invasive organisms pose a global threat and are exceptionally difficult to eradicate after they become abundant in their new habitats. We report a successful multitactic strategy for combating the pink bollworm (Pectinophora gossypiella), one of the world's most invasive pests. A coordinated program in the southwestern United States and northern Mexico included releases of billions of sterile pink bollworm moths from airplanes and planting of cotton engineered to produce insecticidal proteins from the bacterium Bacillus thuringiensis (Bt). An analysis of computer simulations and 21 y of field data from Arizona demonstrate that the transgenic Bt cotton and sterile insect releases interacted synergistically to reduce the pest's population size. In Arizona, the program started in 2006 and decreased the pest's estimated statewide population size from over 2 billion in 2005 to zero in 2013. Complementary regional efforts eradicated this pest throughout the cotton-growing areas of the continental United States and northern Mexico a century after it had invaded both countries. The removal of this pest saved farmers in the United States $192 million from 2014 to 2019. It also eliminated the environmental and safety hazards associated with insecticide sprays that had previously targeted the pink bollworm and facilitated an 82% reduction in insecticides used against all cotton pests in Arizona. The economic and social benefits achieved demonstrate the advantages of using agricultural biotechnology in concert with classical pest control tactics.

Validation of a Landscape-Based Model for Whitefly Spread of the Cucurbit Yellow Stunting Disorder Virus to Fall Melons.

The cucurbit yellow stunting disorder virus (CYSDV) transmitted by Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) has caused significant reductions in fall melon (Cucumis melo L.) yields in Yuma County, Arizona. In a recent landscape-based study, we found evidence that cotton and spring melon fields increased abundance of B. tabaci and spread of CYSDV infection in fall melon fields. Here, we show that a statistical model derived from data collected in 2011-2012 and based on areas of cotton and spring melon fields located within 1,500 m from edges of fall melon fields was sufficient to retrospectively predict incidence of CYSDV infection in fall melon fields during 2007-2010. Nevertheless, the slope of the association between areas of spring melon fields and incidence of CYSDV infection was three times smaller in 2007-2010 than in 2011-2012, whereas the slope of the association between areas of cotton fields and incidence of CYSDV infection was consistent between study periods. Accordingly, predictions were more accurate when data on areas of cotton alone were used as a basis for prediction than when data on areas of cotton and spring melons were used. Validation of this statistical model confirms that crop isolation has potential for reducing incidence of CYSDV infection in fall melon fields in Yuma County, although isolation from cotton may provide more consistent benefits than isolation from spring melon.

Large-Scale Evaluation of Association Between Pheromone Trap Captures and Cotton Boll Infestation for Pink Bollworm (Lepidoptera: Gelechiidae).

Although transgenic cotton producing insecticidal proteins from Bacillus thuringiensis (Bt) is a cornerstone for pink bollworm control in some countries, integrated pest management remains important for bolstering sustainability of Bt cotton and is critical for controlling pink bollworm where Bt cotton is not available or where this pest has evolved resistance to Bt cotton. Here, we used data on moth captures in gossyplure-baited pheromone traps and boll infestations for 163 Bt and 152 non-Bt cotton fields from Arizona to evaluate accuracy of chemical control decisions relying on moth trapping data and capacity of Bt cotton to suppress survival of offspring produced by moths. Assuming an economic injury level of 12% boll infestation, the accuracy of decisions based on moth captures corresponding to economic thresholds of 6%, 8%, and 10% boll infestation increased from 44.7% to 67.1%. The association between moth captures and boll infestation was positive and significant for non-Bt cotton fields but was not significant for Bt cotton fields. Although chemical control decisions based on trapping data were only moderately accurate, pheromone traps could still be valuable for determining when moth populations are high enough to trigger boll sampling to more rigorously evaluate the need for insecticide sprays.

Sustained susceptibility of pink bollworm to Bt cotton in the United States.

Evolution of resistance by pests can reduce the benefits of transgenic crops that produce toxins from Bacillus thuringiensis (Bt) for insect control. One of the world's most important cotton pests, pink bollworm (Pectinophora gossypiella), has been targeted for control by transgenic cotton producing Bt toxin Cry1Ac in several countries for more than a decade. In China, the frequency of resistance to Cry1Ac has increased, but control failures have not been reported. In western India, pink bollworm resistance to Cry1Ac has caused widespread control failures of Bt cotton. By contrast, in the state of Arizona in the southwestern United States, monitoring data from bioassays and DNA screening demonstrate sustained susceptibility to Cry1Ac for 16 y. From 1996-2005, the main factors that delayed resistance in Arizona appear to be abundant refuges of non-Bt cotton, recessive inheritance of resistance, fitness costs associated with resistance and incomplete resistance. From 2006-2011, refuge abundance was greatly reduced in Arizona, while mass releases of sterile pink bollworm moths were made to delay resistance as part of a multi-tactic eradication program. Sustained susceptibility of pink bollworm to Bt cotton in Arizona has provided a cornerstone for the pink bollworm eradication program and for integrated pest management in cotton. Reduced insecticide use against pink bollworm and other cotton pests has yielded economic benefits for growers, as well as broad environmental and health benefits. We encourage increased efforts to combine Bt crops with other tactics in integrated pest management programs.

Suppressing resistance to Bt cotton with sterile insect releases.

Genetically engineered crops that produce insecticidal toxins from Bacillus thuringiensis (Bt) are grown widely for pest control. However, insect adaptation can reduce the toxins' efficacy. The predominant strategy for delaying pest resistance to Bt crops requires refuges of non-Bt host plants to provide susceptible insects to mate with resistant insects. Variable farmer compliance is one of the limitations of this approach. Here we report the benefits of an alternative strategy where sterile insects are released to mate with resistant insects and refuges are scarce or absent. Computer simulations show that this approach works in principle against pests with recessive or dominant inheritance of resistance. During a large-scale, four-year field deployment of this strategy in Arizona, resistance of pink bollworm (Pectinophora gossypiella) to Bt cotton did not increase. A multitactic eradication program that included the release of sterile moths reduced pink bollworm abundance by >99%, while eliminating insecticide sprays against this key invasive pest.