From the Cover: 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.

Invasive life forms pose a major global threat and are especially difficult to eradicate after they become widespread and abundant in their new habitats (1–4). The pink bollworm (Pectinophora gossypiella), one of the world’s most invasive insects, is a voracious lepidopteran pest of cotton that was first detected in the United States in 1917 (5–8). For most of the past century, it was particularly destructive in the southwestern United States, including Arizona, where its larvae fed almost exclusively on cotton, consuming the seeds inside bolls and disrupting lint production (6, 8). In 1969, its peak seasonal density at an Arizona study site was 1.8 million larvae per hectare (ha), which translates to over 200 billion larvae in the 126,000 ha of cotton planted statewide that year (9, 10). In 1990, this pest cost Arizona cotton growers $48 million, including $32 million damage to cotton despite $16 million spent for insecticides sprayed to control it (11). In several field trials, mass releases of sterile pink bollworm moths to mate with wild moths reduced progeny production somewhat, yet did not suppress established populations because the sterile moths did not sufficiently outnumber the wild moths (6, 12–14).Pink bollworm control was revolutionized in 1996 by the introduction of cotton genetically engineered to produce insecticidal proteins from the bacterium Bacillus thuringiensis (Bt). Bt proteins kill some major insect pests yet are not toxic to most nontarget organisms, including people and many beneficial insects (15–17). Transgenic Bt cotton helped to reduce the total annual cost of pink bollworm damage and insecticide treatments to $32 million in the United States (18). Although Bt cotton kills essentially 100% of susceptible pink bollworm larvae (19–21), this pest rapidly evolved resistance to Bt proteins in laboratory selection experiments in Arizona and in Bt cotton fields in India (20–24). To delay the evolution of resistance to Bt cotton, farmers in Arizona planted “refuges” of non-Bt cotton that yielded abundant susceptible moths to mate with the rare resistant moths emerging from Bt cotton (Fig. 1A). The refuge strategy, which has been mandated in the United States and many other countries, but was not adopted widely by farmers in India, helped preserve pink bollworm susceptibility to Bt cotton in Arizona from 1996 to 2005 (24).Open in a separate windowFig. 1.Management strategies. (A) The refuge strategy is the primary approach adopted worldwide to delay the evolution of pest resistance to Bt crops and was used in Arizona from 1996 to 2005. Refuges of non-Bt cotton planted near Bt cotton produce abundant susceptible moths (blue) to mate with the rare resistant moths (red) emerging from Bt cotton. If the inheritance of resistance to Bt cotton is recessive, as in pink bollworm, the heterozygous offspring from matings between resistant and susceptible moths die when they feed on Bt cotton bolls as larvae (24). (B) Bt cotton and sterile moth releases were used together in Arizona from 2006 to 2014 as part of a multitactic program to eradicate the pink bollworm. Susceptible sterile moths (brown) were released from airplanes to mate with the rare resistant moths emerging from Bt cotton. The few progeny produced by such matings (48) are expected to be heterozygous for resistance and to die when they feed on Bt cotton bolls as larvae.As part of a coordinated, multitactic effort to eradicate the pink bollworm from the southwestern United States and northern Mexico, a new strategy largely replacing refuges with mass releases of sterile pink bollworm moths was initiated in Arizona during 2006 (Fig. 1B; 24–27). To enable this novel strategy, the US Environmental Protection Agency granted a special exemption from the refuge requirement, which allowed Arizona cotton growers to plant up to 100% of their cotton with Bt cotton (28). We previously reported data from 1998 to 2009 showing that this innovative strategy sustained susceptibility of pink bollworm to Bt cotton while reducing the pest’s population density (25). Here, to test the idea of eradicating pink bollworm with the combination of Bt cotton and sterile releases, we conducted computer simulations and analyzed field data collected in Arizona from 1998 to 2018.