Extensive cultivation of crops genetically engineered to produce insecticidal proteins from the bacterium Bacillus thuringiensis (Bt) has suppressed some major pests, reduced insecticide sprays, enhanced pest control by natural enemies, and increased grower profits. However, these benefits are being eroded by evolution of resistance in pests. We report a strategy for combating resistance by crossing transgenic Bt plants with conventional non-Bt plants and then crossing the resulting first-generation (F1) hybrid progeny and sowing the second-generation (F2) seeds. This strategy yields a random mixture within fields of three-quarters of plants that produce Bt toxin and one-quarter that does not. We hypothesized that the non-Bt plants in this mixture promote survival of susceptible insects, thereby delaying evolution of resistance. To test this hypothesis, we compared predictions from computer modeling with data monitoring pink bollworm (Pectinophora gossypiella) resistance to Bt toxin Cry1Ac produced by transgenic cotton in an 11-y study at 17 field sites in six provinces of China. The frequency of resistant individuals in the field increased before this strategy was widely deployed and then declined after its widespread adoption boosted the percentage of non-Bt cotton plants in the region. The correspondence between the predicted and observed outcomes implies that this strategy countered evolution of resistance. Despite the increased percentage of non-Bt cotton, suppression of pink bollworm was sustained. Unlike other resistance management tactics that require regulatory intervention, growers adopted this strategy voluntarily, apparently because of advantages that may include better performance as well as lower costs for seeds and insecticides.

https://www.pnas.org/content/pnas/114/21/5413.full.pdf

Hybridizing transgenic Bt cotton with non-Bt cotton counters resistance in pink bollworm

Both maize and cotton genetically engineered to express Bt toxins are widely planted and important pest management tools in the United States. Recently, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) has developed resistance to two toxin Bt maize and cotton (Cry1A and Cry2A). Hence, growers are transitioning to three toxin Bt cotton and maize that express both Cry toxins and the Vip3Aa toxin. H. zea susceptibility to Vip3Aa is threatened by 1) a lack of availability of non-Bt refuge crop hosts, including a 1-5% annual decline in the number of non-Bt maize hybrids being marketed; 2) the ineffectiveness of three toxin cultivars to function as pyramids in some regions, with resistance to two out of three toxins in the pyramid; and 3) the lack of a high dose Vip3Aa event in cotton and maize. We propose that data should be collected on current Cry-resistant H. zea in the field to inform future Bt resistance models and that the deployment of Bt toxins and non-Bt refuge crops should be adjusted to favor susceptibility of H. zea to Bt toxins such as Vip3Aa. Finally, maize growers should be incentivized to plant non-Bt structured refuge and have access to hybrids with high-yielding genetic potential at a reasonable price.

Bt Resistance Implications for Helicoverpa zea (Lepidoptera: Noctuidae) Insecticide Resistance Management in the United States.

Blended refuge for transgenic plants expressing Bacillus thuringiensis (Bt) toxins has been approved in the northern United States as a resistance management strategy alternative to a structured refuge. A three-year study (2012–2014) was conducted with 54 trials across nine states in the southern United States to evaluate plant injury from lepidopteran pests of corn and yield in a corn hybrid expressing Cry1F × Cry1Ab × Vip3Aa20 (Pioneer Brand Optimum Leptra) planted as a pure stand and in refuge blends of 5, 10, and 20% in both early and late plantings. Injury by corn earworm, Helicoverpa zea Boddie (Lepidoptera: Noctuidae), and fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), was generally proportional to the percentage of non-Bt corn within each refuge blend. Across locations, ear injury in plots with 100% Cry1F × Cry1Ab × Vip3Aa20 (Optimum Leptra) corn ranged from no injury to a maximum of 0.42 cm2 per ear in Mississippi in 2013. Leaf injury ratings in 100% non-Bt plots in early and late planted trials in 2014 were 86- and 70-fold greater than in 100% Cry1F × Cry1Ab × Vip3Aa20 (Optimum Leptra) plots. Plants in plots with blended refuges had significantly greater leaf injury in 2012 (5, 10, and 20% refuge blends), in the early-planted corn in 2013 (10 and 20% only), and in both early- and late-planted corn in 2014 (20% only) as compared with leaf injury in a pure stand of Cry1F × Cry1Ab × Vip3Aa20 (Optimum Leptra) seen during these years. Corn ears in plots with blended refuges also had significantly greater area of kernels injured in 2012 (5, 10, and 20%), in early- and late-planted corn in 2013 (5, 10, and 20%), and in early (10 and 20% only)- and late-planted corn (5, 10, and 20%) in 2014 as compared with ear injury in a pure stand of Cry1F × Cry1Ab × Vip3Aa20 (Optimum Leptra) seen during these years. Infestations of southwestern corn borer, Diatraea grandiosella Dyar (Lepidoptera: Crambidae), were also significantly reduced by Cry1F × Cry1Ab × Vip3Aa20 (Optimum Leptra). Despite these differences in injury, yield averaged across locations varied among refuge blends only in the late-planted trials in 2013, with greater yields in the 0% refuge blend than in the 20% blend; however, when examining yield separately by location, only two of nine locations had higher yields in the 100% Bt plots than in any of the blended refuge plots. As a complement to studying the contribution of blended refuge to delaying resistance, quantifying injury and yield in a range of refuge blends is a necessary step to provide management information on the range of lepidopteran pests that occur in the southern United States.

Impact of Lepidoptera (Crambidae, Noctuidae, and Pyralidae) Pests on Corn Containing Pyramided Bt Traits and a Blended Refuge in the Southern United States.

In this review, we evaluate the intentional mixing or blending of insecticidal seed with refuge seed for managing resistance by insects to insecticidal corn (Zea mays). We first describe the pest biology and farming practices that will contribute to weighing trade-offs between using block refuges and blended refuges. Case studies are presented to demonstrate how the trade-offs will differ in different systems. We compare biological aspects of several abstract models to guide the reader through the history of modeling, which has played a key role in the promotion or denigration of blending in various scientific debates about insect resistance management for insecticidal crops. We conclude that the use of blended refuge should be considered on a case-by-case basis after evaluation of insect biology, environment, and farmer behavior. For Diabrotica virgifera virgifera, Ostrinia nubilalis, and Helicoverpa zea in the United States, blended refuge provides similar, if not longer, delays in the evolution of resistance compared to separate block refuges.

Blended Refuge and Insect Resistance Management for Insecticidal Corn.

The fall armyworm, Spodoptera frugiperda (J. E. Smith) and the corn earworm, Helicoverpa zea (Boddie) are among the main pests of maize. Both species exhibit cannibalistic behavior and quite often share the same feeding guild in maize (maize ears), which can result in several interspecific and intraspecific interactions. Paired interaction scenarios of intraspecific and interspecific larvae were assessed in arenas in the presence and absence of food to characterize movements resulting from interactions of these insects. There was a difference in the frequency of behavioral movements in all the interactions, except for S. frugiperda in the presence of food. Head touching and recoiling were the predominant movements in most of the interaction scenarios. Spodoptera frugiperda exhibited a predominance of defensive movements when competing against H. zea in the same instars. Cannibalism and predation occurred frequently in interactions involving 6th instar of H. zea against opponents in 4th instar. Larvae of H. zea show a higher aggressive movement than S. frugiperda. The larvae of S. frugiperda take advantage during the interactions, although they present more defensive movements compared to H. zea. This study provides relevant information regarding the interaction of these species and intraguild interaction, which might influence the population dynamics and the competitive displacement of pest species that share the same ecological niche.

/pdf/attack-and-defense-movements-involved-in-the-interaction-of-ask06r0etw.pdf

Attack and defense movements involved in the interaction of Spodoptera frugiperda and Helicoverpa zea (Lepidoptera: Noctuidae)

ABSTRACT In 2012 and 2013, field trials were conducted near Rosemount, MN, to assess the movement and development of Helicoverpa zea (Boddie) larvae on non-Bt refuge corn plants within a seed mixture of non-Bt and Bt corn. The Bt corn hybrid expressed three Bt toxins—Cry1Ab, Cry1F, and Vip3A. As the use of seed mixtures for insect resistance management (IRM) continues to be implemented, it is necessary to further characterize how this IRM approach impacts resistance development in ear-feeding Lepidopteran pests. The potential for Bt pollen movement and cross pollination of the non-Bt ears in a seed mixture may lead to Bt toxin exposure to larvae developing on those refuge ears. Larval movement and development by H. zea, feeding on non-Bt refuge plants adjacent to either transgenic Bt or non-Bt plants, were measured to investigate the potential for unintended Bt exposure. Non-Bt plants were infested with H. zea eggs and subplots were destructively sampled twice per week within each treatment to assess larval development, location, and kernel injury. Results indicate that H. zea larval movement between plants is relatively low, ranging from 2–16% of larvae, and occurs mainly after reaching the second instar. Refuge plants in seed mixtures did not produce equivalent numbers of H. zea larvae, kernel injury, and larval development differed as compared with a pure stand of non-Bt plants. This suggests that there may be costs to larvae developing on refuge plants within seed mixtures and additional studies are warranted to define potential impacts.

INSECTICIDE RESISTANCE AND RESISTANCE MANAGEMENT Bt Maize Seed Mixtures for Helicoverpa zea (Lepidoptera: Noctuidae): Larval Movement, Development, and Survival on Non-transgenic Maize

And W. D. Hutchison

Papers

INSECTICIDE RESISTANCE AND RESISTANCE MANAGEMENT Bt Maize Seed Mixtures for Helicoverpa zea (Lepidoptera: Noctuidae): Larval Movement, Development, and Survival on Non-transgenic Maize