Plant Biotechnology: Current and Potential Impact For Improving Pest Management In U.S. Agriculture An Analysis of 40 Case Studies June 2002

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1 Plant Biotechnology: Current and Potential Impact For Improving Pest Management In U.S. Agriculture An Analysis of 40 Case Studies June 2002 Insect Resistant Cotton (2) Leonard P. Gianessi Cressida S. Silvers Sujatha Sankula Janet E. Carpenter National Center for Food and Agricultural Policy 1616 P Street, NW Washington, DC Phone: (202) Fax: (202) ncfap@ncfap.org Website: Financial support for this study was provided by the Rockefeller Foundation, Monsanto, The Biotechnology Industry Organization, The Council for Biotechnology Information, Grocery Manufacturers of America, and CropLife America.

2 33. Cotton Insect Resistant (2) Production In the US, just over seventeen million bales of cotton (8.2 billion pounds) were harvested from 13 million cotton acres in This acreage is consistent with 1999 cotton acreage and production and represents an increase from the 14 million bales produced on 10.6 million acres in 1998 [23]. Total cotton crop value in 2000 was $4.8 billion. The vast majority of the cotton is upland varieties with a minority of higher value, extra long staple cotton produced in CA, AZ, NM and TX. Currently, seventeen states contribute to US production (see Table 33.1). Lepidopteran Insect Pests The fall armyworm, soybean looper and the beet armyworm are destructive migratory pests of many crops in the southeastern US. Loopers and armyworms overwinter south of the freeze line-in Florida and coastal areas. Large populations also migrate from Central and South America and the Caribbean islands. In California, the beet armyworm overwinters in the soil as a pupa. Primary damage caused by fall armyworms on cotton is from their feeding on the fruit. The larger, more mature larvae may completely devour squares. They feed extensively on blooms and severely damage bolls by eating the interior portions [27]. When compared to the defoliation pattern of other foliage feeding caterpillars, the defoliation pattern of soybean loopers is unusual: soybean loopers feed from the inside out on plant canopy. In a heavy soybean looper population, the outer canopy will appear undamaged until all the lower leaves on the plant are almost destroyed. Once loopers begin feeding on the outer canopy, they can completely defoliate the plant in 36 to 48 hours [28]. Young beet armyworm larvae feed together and gradually disperse as they grow. They skelotenize leaves. Older larvae chew irregular pieces from leaves and may also feed on squares, flowers, and small bolls [29]. 2

3 Large populations of beet armyworms occur in years with dry summers. During these years many of the parasites (wasps and diseases) that help keep beet armyworm populations in check are reduced [30]. Populations of armyworms often increase following the application of insecticides for other pests, which in turn reduce the natural enemy populations [31]. In recent years beet armyworms have become a greater problem in California cotton due to increased planting nearby of other susceptible hosts such as tomatoes [32]. Table 33.2 tracks estimates of infestation levels of beet armyworm/fall armyworm/soybean looper in cotton by state Years with higher than normal infestations in Texas, Oklahoma, and New Mexico are generally the result of drought conditions. In the drought year of 2000 beet armyworms were at their highest level in Texas since 1980 [26]. Some growers sprayed four times to control BAW. In other states such as North Carolina, infestation levels of BAW are dependent on how far north the pest migrates during the season [26]. These migratory pests advance farther in years with higher than normal early season temperatures. There is some concern that Boll Weevil Eradication Program sprays may contribute to outbreaks of beet armyworms, but there is no definitive data to support that possibility [26]. Bt Cotton I Transgenic Bt cotton, expressing the Cry1Ac insecticidal d-endotoxin of Bacillus thuringiensis Berliner, has been commercially available in the United States since Table 33.3 delineates Bt cotton adoption by state in Since then, B. thuringiensis (Bt) cotton has demonstrated remarkable control of some lepidopteran pests, particularly the tobacco budworm and the pink bollworm. Since its release into commercial markets, Bt cotton seldom, if ever, has required supplemental insecticide control for these two pests [3]. Control of the bollworm has been less dependable, and economically damaging 3

4 infestations of this pest can occur on Bt cotton, particularly after plants have begun flowering and when insecticides have disrupted populations of predators and parasites. The bollworm is inherently more tolerant than tobacco budworm to the Cry1Ac d- endotoxin expressed in currently available Bt cultivars. Additionally, low expression of the toxin in some plant parts, such as in pollen and petals, has been implicated in increased survival of the bollworms on Bt cotton [3]. Other common lepidopteran pests such as fall armyworms, beet armyworms and soybean loopers are even more tolerant than bollworms to Cry1Ac. Bollgard cottons in North Carolina frequently require supplemental bollworm control with insecticides. The major bollworm flight to cotton occurs in North Carolina in late July to early August. The invasion period coincides with the observed drop in average levels of Cry1Ac in cotton fruit [17]. Supplemental foliar insecticide applications (e.g., pyrethroids) have been used in many Bt cotton fields to control economically damaging populations of fall armyworms, beet armyworms, soybean loopers and especially bollworms [2]. Table 33.4 lists the insecticides recommended for budworm/bollworm control. The average use rate for these insecticides is.25 lb AI/A. Table 33.5 displays estimates of current Bt cotton acreage treated with insecticides specifically for supplemental bollworm control. Approximately 36% of current Bt cotton acreage is treated (1.9 million acres) with pounds of chemical active ingredients. Cotton yield losses to bollworms are occurring on current Bt acreage even with the supplemental sprays. In addition, some Bt cotton acreage is not receiving a supplemental spray, and losses are occurring. Table 33.6 delineates cotton losses to bollworms on Bt cotton acreage by state. Approximately bales valued at $19 million were lost to bollworms on Bt cotton acreage in Table 33.7 lists the insecticides recommended for fall armyworm/beet armyworm/soybean looper control. The average use rate for these insecticides is.423 lb AI/A. Table 33.8 displays estimates of current Bt cotton acreage treated with insecticides specifically for beet armyworm/fall armyworm/soybean looper control. Approximately 21% of current Bt cotton acreage is treated with pounds of chemical active 4

5 ingredients. Cotton yield losses to loopers and armyworms are occurring on current Bt acreage even with the supplemental sprays. In addition, some Bt cotton acreage is not receiving a supplemental spray, and losses are occurring. Table 33.9 delineates cotton losses to loopers and armyworms on Bt cotton acreage by state. Approximately bales valued at $3.6 million were lost to loopers/armyworms on Bt cotton acreage in Table summarizes the losses in production volume and value and the costs and amounts of sprays due to bollworms/armyworms/loopers on Bt cotton acreage in Bt Cotton II Unacceptable control of bollworms and other lepidopteran pests such as beet armyworms, fall armyworms and soybean loopers, prompted the development of a new genetically modified cotton that contains two separate crystalline proteins [4]. Bollgard II cotton was developed by incorporating the Cry2Ab protein from Bacillus thuringiensis into a commercially available Bollgard cotton cultivar, Deltapine 50B, which contains the Cry1Ac protein. Bollgard II was produced by particle bombardment, transforming DP50B and adding the Cry2Ab gene [16]. Cloned plants regenerated from the transformed tissue expressed both the Cry1Ac protein and the Cry2Ab protein. These genes also segregated independently [19]. The Cry2Ab protein was added to provide greater insecticidal activity against target pests and broaden the spectrum of total pests controlled. A three-to-six-fold increase was observed in bioactivity of Bollgard II compared with Bollgard against tobacco budworm [4]. Plant expression of Cry2Ab is approximately 10-times higher than for Cry1Ac resulting in an efficacy contribution that is equal to or greater than Cry1Ac on the important lepidopteran insects in US cotton production [14]. The addition of Cry2Ab protein expressed in Bollgard II cotton provides satisfactory control of beet armyworms, fall armyworms, and soybean loopers [2]. Also, efficacy of Bollgard II was improved over Bollgard against bollworms. Field studies indicate that 5

6 Bollgard II cottons will consistently provide satisfactory bollworm control [4]. Researchers observed improved bollworm control in Bollgard II cotton compared with Bollgard cotton during These initial data indicate that Bollgard II will be beneficial in areas where multiple lepidopteran pest species reach economically damaging levels during most years [4]. The dual-toxin cultivars, expressing Cry1Ac and Cry2Ab, may not require supplemental insecticide applications for these pests [3]. Supplemental applications of insecticide may only be necessary for other pests (aphids, sucking bugs, etc.) that are not impacted by proteins in Bollgard II genotypes [7]. In Texas and Arizona, beet armyworm per acre averaged across three sites were 389 for Bollgard II, 11,621 for Bollgard and 24,682 for conventional cotton. Soybean looper larvae numbers and foliage damage was significantly lower for Bollgard II compared to conventional and Bollgard varieties [5]. Very few fall armyworms were found in Bollgard II plots compared to Bollgard or conventional cotton [6]. For fall armyworm, plots containing dual-toxin cotton reduced larvae by 96% over both non-bt and single-toxin cotton in 1999 and Populations of soybean looper were also significantly reduced in plots containing dual-toxin cotton [8]. Reports from field and greenhouse trials conducted in North Carolina demonstrated that Bollgard II genotypes significantly reduced numbers of susceptible and Cry1Ac-tolerant bollworm larvae below that of the Bollgard cottons. These greenhouse data and those from field studies suggest that the commercialization of the dual-gene construct would reduce bollworm damage over that experienced by Bollgard varieties, as well as eliminate the need for supplemental insecticide applications for bollworm control [9]. The data collected in research studies shows that the dual Bt varieties were protected from beet armyworm, tobacco budworm, soybean looper and cabbage looper (see Table 33.11) [12] [11] [6]. 6

7 Bollgard II cotton was evaluated in over 40 small plot field trials across the southeastern states of Alabama, Florida, Georgia, South Carolina, North Carolina and Virginia during the field season of Bollgard II consistently decreased the amount of square and boll damage compared to Bollgard or conventional cotton [13]. In one test, bollworm, beet armyworm and cabbage looper appeared in the field very late in the season. All counts in the Bollgard II were zero and statistically different from Bollgard and DPL 50 [15]. The dual-toxin Bt cultivars will give better control of bollworms than those expressing only Cry1Ac. The control of a large and naturally occurring population of soybean looper by the dual-toxin cultivars was very good (>90%), and it seems unlikely that dualtoxin cultivars (expressing Cry2Ab) would require treatment for this pest [18]. Several field tests on Bollgard II varieties were conducted during the 1999 season in South Carolina. No supplemental treatments were required for Bollgard II cotton genotypes. In conventional cotton, applications were required for bollworm control. Bollgard II cottons show considerable promise of controlling major lepidopterous pests with little need for applications to supplement their control [20]. Data suggest that dual-toxin Bt (Bollgard II) cottons will provide substantially better control of lepidopteran pests compared with the existing, single-toxin Bt cultivars. The superiority of these dual-toxin cultivars will probably be most apparent for soybean looper, beet armyworm and fall armyworm because these species are affected less than bollworm by the existing, single-toxin cultivars [18]. However, control of bollworm populations should also be improved. Estimated Impacts Bollgard cotton will likely be phased out and completely replaced with Bollgard II; a process that will take several years [14]. 7

8 It is estimated that Bt cotton II will be adopted on the same acreage that is currently planted with Bt cotton I at an increased cost of $2/A. The major impact of Bt cotton II would be an elimination of current losses and spraying costs due to bollworms/loopers/armyworms on Bt cotton acreage. These impact estimates are shown in Table It is estimated that Bt cotton would increase cotton production by 37 million pounds with a value of $22 million and reduce pesticide use by pounds. Adoption rates for Bt cotton II may actually be higher than Bt cotton I in California and Texas due to the more widespread infestation of beet armyworms in those states. 8

9 Table 33.1 Cotton Production By State: 2000 Harvested Yield (lbs/a) Production Value (million $) Acres (000) (000 bales/yr.) Alabama Arizona Arkansas California Florida Georgia Kansas Louisiana Mississippi Missouri New Mexico North Carolina Oklahoma South Carolina Tennessee Texas Virginia Total pound bales Source [23] [24] Table 33.2 Acres Infested with Fall Armyworm/Beet Armyworm/Soybean Looper AL AZ AR CA FL GA LA MS MO NM NC OK 17 0 < SC <1 TN 5 2 < < TX VA < Source: [21] 9

10 Table 33.3 Adoption of Bt Cotton by State (2000) Harvested Acres (000) % Bt 1 Bt Acres (000) AL AZ AR CA FL GA LA MS MO NM NC OK SC TN TX VA Total Source: [25] Table 33.4 Insecticides Recommended for Budworm/Bollworm Control (lb/ai A) Acephate 1.00 Bifenthrin 0.06 Cyfluthrin 0.04 Cypermethrin 0.05 Deltamethrin 0.02 Esfenvalerate 0.04 Indoxacarb 0.11 Lambdacyhalothrin 0.03 Methomyl 0.45 Profenofos 1.00 Spinosad 0.08 Thiodicarb 0.60 Tralomethrin 0.02 Zetamethrin 0.04 Average 0.25 Source: [22] 10

11 Table 33.5 Bt Cotton Acreage Sprayed for Bollworms (2000) Bt Acres (000) % Sprayed 1 Bt Acres Sprayed (000) # of Sprays/A $/Spray $/yr. (000) Lbs AI/yr 2 AL AZ AR CA FL GA LA MS MO NM NC OK SC TN TX VA Total [21] Data for 2000 (NC for 2001). California Assigned AZ data 2 Calculated at.25lb AI/A multiplied by the number of sprays per acre. 11

12 Table 33.6 Cotton Losses to Bollworms on Bt Cotton Acreage (2000) Bt Acres (000) Bales Lost 1 per Bt A Total Bales Lost Total Loss 2 ($ 000) AL AZ AR CA FL GA LA MS MO NM NC OK SC TN TX VA Total Derived from [21] for AZ, LA, NC and TN. Assigned to neighboring states. 2 Calculated at $288/Bale. 12

13 Table 33.7 Insecticides Recommended for Soybean Looper, Beet Armyworm, Fall Armyworm (Lb. AI/A) Acephate 1.00 Chlorpyrifos 0.62 Diflubenzuron 0.09 Indoxacarb 0.10 Methomyl 0.40 Profenofos 0.90 Spinosad 0.08 Thiodicarb 0.75 Methoxyfenozide 0.11 Tebufenozide 0.18 Avg Source: [22] 13

14 Table 33.8 Bt Cotton Acreage Sprayed for Fall Armyworm/ Beet Armyworm/Soybean Looper (2000) Bt Acres (000) % Sprayed 1 Bt Acres Sprayed (000) $/Spray Spray Cost $/yr. (000) Lbs AI/yr 2 AL AZ AR CA FL GA LA MS MO NM NC OK SC TN TX VA Total Derived from [21]. Estimates for AZ, LA, NC and TN are specific for Bt acreage. Estimates for other states are derived from statewide data. Data for 2000 except TN (1999) and NC (2001). California estimates assigned from AZ. 2 Calculated at.423lb AI/A 14

15 Table 33.9 Cotton Losses to BAW/FAW/SL on Bt Cotton Acreage (2000) Bt Acres (000) Bales Lost Per Bt A 1 Total Bales Lost Total Loss 2 ($ 000/yr) AL AZ AR CA FL GA LA MS MO NM NC OK SC TN TX VA Total Derived from [21] for AZ, LA, NC and TN. Assigned to neighboring states. 2 Calculated at $288/bale. 15

16 Table Summary of Current Losses and Costs on Bt Cotton Acreage (BW/FAW/BAW/SL) BW (bales) Production Volume FAW/BAW/SL Total (bales) (000lbs) Production Value (000 $/yr.) BW FAW/BAW/SL Total AL AZ AR CA FL GA LA MS MO NM NC OK SC TN TX VA BW Sprays Spray Costs (000$) FAW/BAW/SL Sprays Pesticide Use (lbs. AI/yr) Total BW Sprays FAW/BAW/SL Sprays Total AL AZ AR CA FL GA LA MS MO NM NC OK SC TN TX VA

17 Table % Reduction of Larvae by Bt Cottons Bt Cotton I Bt Cotton II Bollworm Tobacco Budworm Soybean Looper Fall Armyworm Beet Armyworm Source: [6]. Reductions are measured from the number of larvae found in a conventional cotton variety. Table Potential Impacts of Adoption of Bt Cotton II 2 Bt Acres (000) Volume (000lbs) Value (000$) Production Sprays (000$) Costs Bt II 1 (000$) Net (000$) Net Income (000$) Pesticide Use Reduction (lbs/yr.) AL AZ AR CA FL GA LA MS MO NM NC OK SC TN TX VA Total Calculated at $2.00/A 2 Data from Table

18 References: 1. Adamczyk, J. J., et al., Susceptibility of Conventional and Transgenic Cotton Bolls Expressing the Bacillus thuringiensis Cry1A(c) d-endotoxin to Fall Armyworm (Lepidoptera: Noctuidae) and Beet Armyworm (Lepidoptera: Noctuidae) Injury, Journal of Agricultural Entomology, 15(3): , July Adamczyk, J. J., et al., Field Efficacy and Seasonal Expression Profiles for Terminal Leaves of Single and Double Bacillus thuringiensis Toxin Cotton Genotypes, Journal of Economic Entomology, 94(6): , Stewart, S. D., et al., Impact of Bt Cottons Expressing One or Two Insecticidal Proteins of Bacillus thuringiensis Berliner on Growth and Survival of Noctuid (Lepidoptera) Larvae, Journal of Economic Entomology, 94(3): , Gore, J., et al., Bollworm (Lepidoptera: Noctuidae) Survival on Bollgard and Bollgard II Cotton Flower Bud and Flower Components, Journal of Economic Entomology, 94(6): , Jost, D. J., Bollgard II Cotton Efficacy Summary Southwest, 2001 Beltwide Cotton Conferences. 6. Adamczyk, J. J., et al., Evaluation of Bollgard II (CV. DP50BII) in the Mississippi Delta: Field Efficacy Against Various Lepidoptera While Profiling Season-Long Expression of Cry1A(c) and Cry2A(b), 2001 Beltwide Cotton Conferences. 7. Ridge, Rebecca, et al., Efficacy of Bollgard II as a Lepidopterous Larvicide in Cotton, 2001 Beltwide Cotton Conferences. 8. Akin, D. S., et al., Field Efficacy of Cotton Expressing Two Insecticidal Proteins of Bacillus thuringiensis, 2001 Beltwide Cotton Conferences. 9. Jackson, R. E., et al., Efficacy of Bollgard and Bollgard II Cottons Against Bollworm, Helicoverpa Zea (Boddie) in Field and Greenhouse Studies, 2001 Beltwide Cotton Conferences. 10. Marsh, B. H., et al., Bollgard II in the Southern San Joaquin Valley, 2001 Beltwide Cotton Conferences. 11. Lorenz, Gus, et al., Bollgard II Performance in Arkansas, 2001 Beltwide Cotton Conferences. 18

19 12. Allen, Charles T. and Marwan S. Karboutli, Effectiveness of Bollgard II Cotton Varieties Against Foliage and Fruit Feeding Caterpillars in Arkansas, 2000 Beltwide Cotton Conferences. 13. Pitts, D. L., Bollgard II Cotton Efficacy Summary Southeast, 2001 Beltwide Cotton Conferences. 14. Voth, R. D., Bollgard II Cotton Technical Review, 2001 Beltwide Cotton Conferences. 15. Norman, John W., et al., Performance of Bollgard II Cotton Against Lepidopterous Pests in the Lower Rio Grande Valley of Texas, 2001 Beltwide Cotton Conferences. 16. Rahn, P. R., et al., Efficacy and Agronomic Performance of Bollgard II, 2001 Beltwide Cotton Conferences. 17. Jackson, R. E., et al., Field and Greenhouse Performance of Bollworm on Bollgard II Cotton Genotypes, 2000 Beltwide Cotton Conferences. 18. Stewart, S. D. and K. S. Knighten, Efficacy of Bt Cotton Expressing Two Insecticidl Proteins of Bacillus thuringiensis Berliner on Selected Caterpillar Pests, 2000 Beltwide Cotton Conferences. 19. Greenplate, J. T., et al., Bollgard II Efficacy: Quantification of Total Lepidopteran Activity in a 2-Gene Product, 2000 Beltwide Cotton Conferences. 20. Ridge, R. L., et al., Field Comparison of Genetically-Modified Cottons Containing One Strain (Bollgard) and Two Strains (Bollgard II) of Bacillus thuringiensis kurstaki, 2000 Beltwide Cotton Conferences. 21. Williams, Michael R., Cotton Insect Losses, Beltwide Cotton Conferences, Alabama Pest Management Handbook, Extension Service, Clemson University. 23. USDA, Crop Production 2000 Summary, National Agricultural Statistics Service, January USDA, Crop Values 2000 Summary, National Agricultural Statistics Service, February

20 25. USDA, Cotton Varieties Planted (Annual ), Agricultural Marketing Service-Cotton Program, Memphis Tennessee. 26. Hardee, D. D., et al, Annual Conference Report on Cotton Insect Research and Control, Beltwide Cotton Conferences, Smith, H. and Barry L. Freeman, Fall Armyworms: Consistent Cotton Pests, Agricultural & Natural Resources Entomology, circular ANR Smith, Ronald H., Soybean Loopers: Late Season Foliage Feeders on Cotton, Alabama Cooperative Extension Service, June Integrated Pest Management for Cotton in the Western Region of the United States, University of California, Division of Agriculture and Natural Resources, Publication 3305, Smith, R. H., et al, Diseases, Parasites Help Control Beet Armyworms in Cotton, Highlights of Agricultural Research, Alabama Agricultural Experiment Station, Summer Moulton, J. K., et al, Studies of Resistance of Beet Armyworm (Spodoptera Exigua) to Spinosad in Field Populations from the Southern USA and Southeast Asia, 1999 Beltwide Cotton Conferences. 32. A New Look at the Beet Armyworm, California-Arizona-Texas Cotton Magazine, April

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