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CONSIDERATIONS OF ADOPTING BT SEED MIXTURE STRATEGY FOR CABBAGE LOOPER In 1996, commercialization of first generation transgenic cotton that expresses Bacillus thuringiensis (Bt) toxins was approved by the US EPA. This Bt cotton was effective against many lepidopteran pests, including Heliothis virescens (Fabricius), Helicoverpa zea (Boddie) and Pectinophora gossypiella (Saunders). Since that time the acreage of cultivated Bt cotton has increased rapidly around the world. However, growing Bt cotton successively raises the potential for resistance adaptation of target insects to the Bt toxins.1 Although no Bt crop-resistant lepidopteran pest populations have yet been documented under field conditions, some authors have reported the failing or decreased effectiveness of Bt cotton against some insect pests.2,3,4 In addition, several species have developed resistance to Bt toxins in laboratory selection experiments.5 In 2002, transgenic cotton that simultaneously expresses two Bt toxins, Cry1Ac and Cry2Ab, was approved for commercial use. Although this line is more effective than single toxin Bt cotton in protecting cotton from damage by lepidopteran pests, adaptation by the target pests is still a concern.6 Seed mixture strategy has been proposed to delay the evolution of adaptation of insects to Bt toxins.7 However, Mallet and Porter8 warned that seed mixtures of toxic and toxin-free plants within fields would hasten the development of resistance if insect movement was independent of the toxin inside plants. Tabashnik9 later countered that seed mixtures could delay resistance of insects to Bt toxins regardless of whether insect movement is independent of the toxin inside the plant. However, based on the field experiments with diamondback moth, Plutella xylostella (L.), Shelton et al.10 did not endorse seed mixtures as a strategy to delay evolution of resistance to Bt toxins. Ramachandran et al.11,12 reported that movement of P. xylostella between conventional and transgenic canola plants is independent of toxin. Furthermore, P. xylostella larvae have been shown to move to toxic plants from toxin-free plants if the population density on toxin-free plants was greater than that on toxic plants.13 So movement of insects between Bt plants and non-Bt plants seems to be an important factor in adapting Bt toxins of insect pests. Cabbage looper, Trichoplusia ni, is one of the most serious pests of cruciferous vegetables and a secondary pest of cotton. It has great potential to develop resistance to Bt toxins.14 In southern Texas, cotton is planted from February to March, and grows in the field until late August. Cabbage can be planted side by side with cotton, and the two crops share many common insect pests. It is a common phenomenon that T. ni migrates from cabbage to cotton fields and vice versa. We conducted a series of laboratory experiments to investigate the behavior response of cabbage looper larvae, originating from cabbage, to a mixture of Bollgard II (expressing Cry1Ac and Cry2Ab) and non-Bt cotton leaves.15 We also determined the effects of the mixture of Bollgard II and non-Bt cotton leaves on development of cabbage looper larvae. Our results indicate that young cabbage looper larvae were able to detect Bt cotton leaves and non-Bt cotton leaves. When the larvae were exposed to non-Bt leaves, all larvae moved to the inner part of the cotton leaves and fed there. In contrast, most larvae moved off or on the edge of the leaves (attempted escaping) when exposed to Bollgard II leaves only. When exposed to a mixture of Bollgard II and non-Bt leaves, most larvae moved to and located on the non-Bt leaves. These results indicate that young cabbage looper larvae distinguished and avoided or attempted to avoid Bt cotton leaves. The movement of T. ni larvae between Bt and non-Bt leaves was generally unidirectional, i.e., from Bt cotton leaves to non-Bt cotton leaves, and not vice versa. Some larvae did move to Bollgard II leaves, but fed only a little (1.8 mm2 per larva compared with 22.6 mm2 per larva in the control). The results indicate that the larvae moved to the Bt leaves and initiated feeding, but could not subsequently sustain feeding, and moved either to non-Bt cotton leaves or off the cotton leaves. These results were further supported by the fact that the pupae that developed from larvae that were exposed to a mixture of Bollgard II and non-Bt cotton leaves were significantly smaller than those developed from larvae that were exposed only to non-Bt cotton leaves. The difference in total development times between male and female cabbage looper larvae and pupae fed on non-Bt cotton leaves compared to a mixture of non-Bt and Bt cotton leaves was less than 2 d, which would probably not be long enough to cause assortative mating between two populations. This result also implies that development of cabbage looper larvae is not affected as much as other lepidopteran species. Liu et al.16 found that a resistant strain of larvae of the pink bollworm, Pectinophora gossypiella, grown on Bt cotton takes 5.7 d longer to develop than susceptible larvae on non-Bt cotton. They suggested that the developmental asynchrony between the initially rare homozygous resistant adults and the more abundant homozygous susceptible adults emerging from non-Bt plants favors non-random mating and could reduce the expected benefits of the refuge strategy. Under field conditions, lepidopteran larvae are capable of migrating from one plant to another, especially when plants are large and are touching each other; hence, non-Bt plants mixed with Bt plants may not be easily protected. In addition, if larvae that feed on Bt plants can move to non-Bt plants to complete their development, the risk of evolving resistance is increased. Another concern is that in some localities such as southern Texas, Bt insecticides are widely used on vegetables and many other crops to protect from cabbage looper damage, and Bt-resistant cabbage looper has been detected.16 Therefore, under field conditions in southern Texas it is possible that the cabbage looper could develop resistance to both Bt transgenic cotton and the Bt insecticides used on vegetable crops. The merit of Bt and non-Bt seed mixtures at planting as a resistance management strategy needs further evaluation as part of ongoing efforts to evaluate the effects of the Bt toxins in cotton on cabbage looper and other pests. Sources 2. Adamczyk JJ Jr et al. (1998) Larval survival and development of the fall armyworm (Lepidoptera: Noctuidae) on normal and transgenic cotton expressing the Bacillus thuringiensis Cry1A(c) –endotoxin. J. Econ. Entomol. 91, 539-545 3. Burd T et al. (1999) Performance of selected Bt cotton genotypes against bollworm in North Carolina. 1999 Beltwide Cotton Conference, Orlando, USA, 3-7 January, 1999: Volume 1. National Cotton Council, Memphis, USA. 931-934 4. Allen C T et al. (2000) Effectiveness of Bollgard II cotton varieties against foliage and fruit feeding caterpillars in Arkansas. (2000) Proceedings Beltwide Cotton Conferences, San Antonio, USA, 4-8 January, 2000: Volume 2. National Cotton Council, Memphis, TN, USA. 1093-1094 5. Tabashnik B E et al. (2003) Insect resistance to transgenic Bt crops: Lessons from the laboratory and field. J. Econ. Entomol. 96: 1031-1038 6. Gould F (2003) Bt-resistance management—theory meets data. Nature Biotechnol. 21, 1450 – 1451 7. Gould F & Anderson A. (1991) Effects of Bacillus thuringiensis and HD-73 delta-endotoxin on growth, behavior, and fitness of susceptible and toxin-adapted strains of Heliothis virescens (Lepidoptera: Noctuidae). Environ. Entomol. 20, 30-38 8. Mallet J & Porter P. (1992) Preventing insect adaptation to insect-resistant crops: are seed mixtures or refugia the best strategy? Proc. R. Soc. Lond. B. 250, 165-169 9. Tabashnik B. (1994) Delaying insect adaptation to transgenic plants: seed mixtures and refugia reconsidered. Proc. R. Soc. L. B. 255, 7-12 10. Shelton A M et al.(2000) Field tests on managing resistance to Bt-engineered plants. Nature Biotechnol. 18, 339-342 11. Ramachandran S et al. (1998a) Movement and survival of diamondback moth (Lepidoptera: Plutellidae) larvae in mixtures of nontransgenic and transgenic canola containing a cryIA(c) gene of Bacillus thuringiensis. Environ. Entomol. 27, 649-656 12. Ramachandran S et al. (1998b) Survival, development, and oviposition of resistant diamondback moth (Lepidoptera: Plutellidae) on transgenic canola producing a Bacillus thuringiensis toxin. J. Econ. Entomol. 91, 1239-1244 13. Kumar H. (2004) Orientation, feeding, and ovipositional behavior of diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae), on transgenic cabbage expressing Cry1Ab toxin of Bacillus thuringiensis (Berliner). Environ. Entomol. 33, 1025-1031 14. Janmaat A F & Myers J. (2003) Rapid evolution and the cost of resistance to Bacillus thuringiensis in greenhouse populations of cabbage looper, Trichoplusia ni. Proc. R. Soc. Lond. B. 270, 2263-2270 15. Li YX, Greenberg SM, Liu TX. (2006) Effects of Bt cotton expressing Cry1ac and Cry2ab and non-Bt cotton on behavior, survival and development of Trichoplusia ni (Lepidoptera: Noctuidae). Crop Protection Journal 25, 940-948 16. Liu Y B et al. (1999) Development time and resistance to Bt crops. Nature 400, 519 T.-X. Liu |