Natural enemies delay insect resistance to Bt crops

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Liu, Xiaoxia ^a,b   Chen, Mao ^b,f   Collins, Hilda L ^b   Onstad, David W ^c,g   Roush, Richard T ^d   Zhang, Qingwen ^a   Earle, Elizabeth D ^e   Shelton, Anthony M ^b  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b New York State Agricultural Experiment Station   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e Department of Obstetrics Gynecology   (United States)

^f MONSANTO COMPANY   (United States)

^g DUPONT COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRY1AC TOXIN; SPINOSAD;

ADULT; ANIMAL EXPERIMENT; ARTICLE; BACILLUS THURINGIENSIS; BIOLOGICAL CONTROL AGENT; BROCCOLI; COCCINELLIDAE; COLEOMEGILLA MACULATA; CONTROLLED STUDY; DEFOLIATION; FEMALE; INSECT CONTROL; INSECT RESISTANCE; INTEGRATED PEST MANAGEMENT; MALE; NATURAL ENEMY; NONHUMAN; PLANT DAMAGE; PLANT INSECT INTERACTION; PLANT PEST INTERACTION; PLANT RESPONSE; PLUTELLA XYLOSTELLA; POPULATION DENSITY; PREDATOR PREY INTERACTION; PROTEIN EXPRESSION; SURVIVAL RATE; ANIMAL; CROP; GENETICS; INSECT; INSECTICIDE RESISTANCE; PHYSIOLOGY;

ANIMALS; BACILLUS THURINGIENSIS; CROPS, AGRICULTURAL; INSECTICIDE RESISTANCE; INSECTS;

EID: 84896997145     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0090366     Document Type: Article

References (46)

1. Shelton AM, Zhao J-Z, Roush RT (2002) Economic, ecological, food safety, and social consequences of the deployment of Bt transgenic Plants. Annu Rev Entomol 47: 845-881. (Pubitemid 34108597)
2. Romeis J, Shelton AM, Kennedy GG (2008) Integration of insect-resistant genetically modified crops within IPM programs. Dordrecht, Springer. 441 pp.
3. James C (2012) Global status of commercialized transgenic crops: Bt cotton, ISAAA Briefs No. 44. Ithaca, NY: International Service for the Acquisition of Agri-biotech Applications.
4. Qaim M, Pray CE, Zilberman D (2008) Economic and social considerations in the adoption of Bt crops. In: Romeis J, Shelton AM, Kennedy GG, editors. Integration of insect-resistant genetically modified crops within IPM programs. Dordrecht: Springer. pp 329-356.
5. Kathage J, Qaim M (2012) Economic impacts and impact dynamics of Bt cotton in India. Proc Natl Acad Sci USA 109: 11652-11656.
6. Lu Y, Wu K, Jiang Y, Guo Y, Desneux N (2012) Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 487: 362-365.
7. Carrière Y, Ellers-Kirk C, Sisterson M, Antilla L, Whitlow M, et al. (2003) Long-term regional suppression of pink bollworm by Bacillus thuringiensis cotton. Proc Natl Acad Sci USA 100: 1519-1523. (Pubitemid 36254479)
8. Wu KM, Lu YH, Feng HQ, Jiang YY, Zhao J-Z (2008) Suppression of cotton bollworm in multiple crops in China in areas with Bt toxin-containing cotton. Science 321: 1676-1678.
9. Hutchison WD, Burkness EC, Mitchell PD, Moon RD, Leslie TW, et al. (2010) Areawide suppression of European corn borer with Bt maize reaps savings to non-Bt maize growers. Science 330: 222-225.
10. Naranjo SE (2009) Impacts of Bt crops on non-target organisms and insecticide use patterns. CAB Reviews: Perspectives in agriculture, veterinary science, nutrition and natural resources 4: No.011. DOI: 10.1079/ PAVSNNR20094011.
11. Gould F (1998) Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annu Rev Entomol 43: 701-726.
12. Onstad DW (2008) The future of insect resistance management. In: Onstad DW, editor. Insect resistance management: biology, economics and prediction. London: Academic Press. pp. 289-300.
13. Van Rensburg JBJ (2007) First report of field resistance by stem borer, Busseola fusca (Fuller) to Bt-transgenic maize. S African J Plant Soil 24: 147-151.
14. Storer NP, Babcock JM, Schlenz M, Meade T, Thompson GD, et al. (2010) Discovery and characterization of field resistance to Bt maize: Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico. J Econ Entomol 103: 1031-1038.
15. Dhurua S, Gujar GT (2011) Field-evolved resistance to Bt toxin Cry1Ac in the pink bollworm, Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae) from India. Pest Manag Sci 67: 898-903.
16. Gassmann AJ, Petzold-Maxwell JL, Keweshan RS, Dunbar MW (2011) Field-evolved resistance to Bt maize by western corn rootworm. PLoS ONE 6(7): e22629.
17. Bates SL, Zhao JZ, Roush RT, Shelton AM (2005) Insect resistance management in GM crops: past, present and future. Nat Biotechnol 23: 57-62. (Pubitemid 41724625)
18. Tabashnik BE, Van Rensburg JBJ, Carrière Y (2009) Field-evolved insect resistance to Bt crops: definition, theory, and data. J Econ Entomol 102: 2011-2025.
19. Huang F, Andow D, Bushman LL (2012) Success of the high-dose/refuge resistance management strategy after 15 years of Bt crop use in North America. Entomol Exp Appl 140: 1-16.
20. Wolfenbarger LL, Naranjo SE, Lundgren JG, Bitzer RJ, Watrud LS (2008) Bt crops effects on functional guilds of non-target arthropods: a meta-analysis. PLoS ONE 3(5): e2284. DOI:10.1371/journal.pone.0002118.
21. Desneus N, Bernal JS (2010) Genetically modified crops deserve greater ecotoxicological scrutiny. Ecotoxicology 19: 1642-1644.
22. Romeis J, McLean MA, Shelton AM (2013) When bad science makes good headlines: the case of Bt maize and regulatory bans. Nat Biotechnol 37: 386-7.
23. Desneus N, Ramirez-Romero R, Bokonon-Ganta AH, Bernal JS (2010) Attraction of the parasitoid Cotesia marginiventris to host (Spodoptera frugiperda) frass is affected by transgenic maize. Ecotoxicology, 19: 1183-1192.
24. Chen M, Zhao JZ, Collins HL, Earle ED, Cao J, et al. (2008) A critical assessment of the effects of Bt transgenic plants on parasitoids. PLoS ONE 3(5): e2284. DOI: 10.1371/journal.pone.0002284.
25. Liu XX, Chen M, Onstad D, Roush R, Shelton AM (2011) Effect of Bt broccoli and resistant genotype of Plutella xylostella (Lepidoptera: Plutellidae) on development and host acceptance of the parasitoid Diadegma insulare (Hymenoptera: Ichneumonidae). Transgenic Res 20: 887-897.
26. Tian JC, Collins HL, Romeis J, Naranjo SE, Hellmich RL, et al. (2012) Using field-evolved resistance to Cry1F maize in a lepidopteran pest to demonstrate no adverse effects of Cry1F on one of its major predators. Transgenic Res 21: 1303-1310.
27. Lovei GL, Andow DA, Arpaia S (2009) Transgenic insecticidal crops and natural enemies: a detailed review of laboratory studies. Environ Entomol 38: 293-306.
28. Shelton AM, Naranjo S, Romeis J, Hellmich RH, Wolt J, et al. (2009) Setting the record straight: a rebuttal to an erroneous analysis on transgenic insecticidal crops and natural enemies. Transgenic Res 18:317-322.
29. Gould F, Kennedy GG, Johnson MT (1991) Effects of natural enemies on the rate of herbivore adaptation to resistant host plants. Entomol Exp Appl 58: 1-14.
30. Johnson MT, Gould F, Kennedy GG (1997) Effects of natural enemies on relative fitness of Heliothis virescens genotypes adapted and not adapted to resistant host plants. Entomol Exp Appl 82: 219-230.
31. Johnson MT, Gould F, Kennedy GG (1997) Effect of an entomopathogen on adaptation of Heliothis virescens populations to transgenic host plants. Entomol Exp Appl 83: 121-135.
32. Mallampalli N, Gould F, Barbosa P (2005) Predation of Colorado potato beetle eggs by a polyphagous ladybeetle in the presence of alternate prey: potential impact on resistance evolution. Entomol Exp Appl 114: 47-54. (Pubitemid 40191489)
33. Heimpel GE, Neuhauser C, Andow DA (2005) Natural enemies and the evolution of resistance to transgenic insecticidal crops by pest insects: the role of egg mortality. Environ Entomol 34: 512-526. (Pubitemid 40778442)
34. Chilcutt CF, Tabashnik BE (1999) Simulation of integration of Bacillus thuringiensis and the parasitoid Cotesia plutellae (Hymenoptera: Braconidae) for control of susceptible and resistant diamondback moth (Lepidoptera: Plutellidae). Environ Entomol 28: 505-512. (Pubitemid 129582393)
35. Arpaia S, Gould F, Kennedy G (1997) Potential impact of Coleomegilla maculata predation on adaptation of Leptinotarsa decemlineata to Bt-transgenic potatoes. Entomol Exp Appl 82: 91-100.
36. Gassmann AJ, Stock SP, Carrière Y, Tabashnik BE (2006) Effect of entomopathogenic nematodes on the fitness cost of resistance to Bt toxin Cry1Ac in pink bollworm (Lepidoptera: Gelechiidae). J Econ Entomol 99: 920-926. (Pubitemid 44638087)
37. Talekar NS, Shelton AM (1993) Biology, ecology and management of the diamondback moth. Annu Rev Entomol 38: 275-301. (Pubitemid 24414262)
38. Liu XX, Chen M, Collins HL, Onstad D, Roush R, et al. (2012) Effect of insecticides and Plutella xylostella (Lepidoptera: Plutellidae) genotype on a predator and parasitoid and implications for the evolution of insecticide resistance. J Econ Entomol 105: 354-362.
39. Lundgren JG, Gassmann AJ, Bernal J, Duan JJ, Ruberson J (2009) Ecological compatibility of GM crops and biological control. Crop Prot 28: 1017-1030.
40. Tang JD, Collins HL, Metz TD, Earle ED, Zhao JZ, et al. (2001) Greenhouse tests on resistance management of Bt transgenic plants using refuge strategies. J Econ Entomol 94: 240-247. (Pubitemid 33749907)
41. Roush RT (1998) Two toxin strategies for management of insecticidal transgenic crops: can pyramiding succeed where pesticide mixtures have not? Phil Trans Royal Soc Lond B 353: 1777-86.
42. Shelton AM, Tang JD, Roush RT, Metz TD, Earle ED (2000) Field tests on managing resistance to Bt-engineered plants. Nat Biotechnol 18: 339-342. (Pubitemid 30159489)
43. Zhao JZ, Cao J, Collins HL, Bates SL, Roush RT, et al. (2005) Concurrent use of transgenic plants expressing a single and two Bacillus thuringiensis genes speeds insect adaptation to pyramided plants. Proc Natl Acad Sci USA 102: 8426-8430. (Pubitemid 40862752)
44. Metz TD, Roush RT, Tang JD, Shelton AM, Earle ED (1995) Transgenic broccoli expressing a Bacillus thuringiensis insecticidal crystal protein: implications for pest resistance management strategies. Mol Breeding 1: 309-317. (Pubitemid 3007923)
45. Zhao J-Z, Collins HL, Shelton AM (2010) Testing insecticide resistance management strategies: mosaic versus rotations. Pest Manag Sci 66: 1101-1105.
46. SPSS (1998) SPSS User's Guide. Chicago, SPSS Inc.