Synergism between entomopathogenic nematodes and Bacillus thuringiensis crops: Integrating biological control and resistance management

Journal of Applied Ecology

Volumn 45, Issue 3, 2008, Pages 957-966

  Gassmann, Aaron J ^a,c   Stock, S Patricia ^a   Sisterson, Mark S ^b   Carrière, Yves ^a   Tabashnik, Bruce E ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b U S DEPARTMENT OF AGRICULTURE   (United States)

^c IOWA STATE UNIVERSITY   (United States)

Author keywords

Cotton; Cry1Ac; Fitness costs; Genetically modified crops; Heterorhabditis bacteriophora; Pectinophora gossypiella; Refuge strategy; Simulation modelling; Steinernema riobrave

Indexed keywords

ADAPTATION; BACTERIUM; BIOCONTROL AGENT; BIOLOGICAL CONTROL; ECOLOGICAL MODELING; ENTOMOPATHOGENIC ORGANISM; EVOLUTION; INTEGRATED PEST MANAGEMENT; MORTALITY; NEMATODE; PEST RESISTANCE; SYNERGISM; TRANSGENIC PLANT;

BACILLUS THURINGIENSIS; BACTERIA (MICROORGANISMS); GOSSYPIUM HIRSUTUM; HETERORHABDITIS BACTERIOPHORA; HEXAPODA; NEMATODA; PECTINOPHORA GOSSYPIELLA; STEINERNEMA RIOBRAVE;

EID: 43149096256     PISSN: 00218901     EISSN: 13652664     Source Type: Journal    
DOI: 10.1111/j.1365-2664.2008.01457.x     Document Type: Article

References (57)

1. Abbott, W.S. (1925) A method of computing the effectiveness of an insecticide. Journal of Economic Entomology, 18, 265 267.
2. Barbercheck, M.E. (1993) Tritrophic level effects on entomopathogenic nematodes. Environmental Entomology, 22, 1166 1171.
3. Barbercheck, M.E., Wang, J. Hirsh, I.S. (1995) Host plant effects on entomopathogenic nematodes. Journal of Invertebrate Pathology, 66, 169 177.
4. Baur, M.E., Kaya, H.K., Tabashnik, B.E. Chilcutt, C.F. (1998) Suppression of diamondback moth (Lepidoptera: Plutellidae) with an entomopathogenic nematode (Rhabditida: Steinernematidae) and Bacillus thuringiensis Berliner. Journal of Economic Entomology, 91, 1089 1095.
5. Bird, L.J. Akhurst, R.J. (2004) Relative fitness of Cry1A-resistant and -susceptible Helicoverpa armigera (Lepidoptera: Noctuidae) on conventional and transgenic cotton. Journal of Economic Entomology, 97, 1699 1709.
6. Bird, L.J. Akhurst, R.J. (2007) Effects of host plant species on fitness costs of Bt resistance in Helicoverpa armigera (Lepidoptera: Noctuidae). Biological Control, 40, 196 203.
7. Boemare, N. (2002) Biology, taxonomy and systematics of Photorhabdus and Xenorhabdus. Entomopathogenic Nematology (ed. R. Gaugler pp. 35 56. CABI Publishing, Wallingford.
8. Bourguet, D., Desquilbet, M. Lemarié, S. (2005) Regulating insect resistance management: the case of non-Bt corn refuges in the US. Journal of Environmental Management, 76, 210 220.
9. Burd, A.D., Gould, F., Bradley, J.R., van Duyn, J.W. Moar, W.J. (2003) Estimated frequency of nonrecessive Bt resistance genes in bollworm, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) in eastern North Carolina. Journal of Economic Entomology, 96, 137 142.
10. Campbell, J.F., Lewis, E.E., Stock, S.P., Nadler, S. Kaya, H.K. (2003) Evolution of host search strategies in entomopathogenic nematodes. Journal of Nematology, 35, 142 145.
11. Caprio, M.A. (2001) Source-sink dynamics between transgenic and non-transgenic habitats and their role in the evolution of resistance. Journal of Economic Entomology, 94, 698 705.
12. Carrière, Y., Ellers-Kirk, C., Biggs, R., Degain, B., Holley, D., Yafuso, C., Evans, P., Dennehy, T.J. Tabashnik, B.E. (2005b) Effects of cotton cultivar on fitness costs associated with resistance of pink bollworm (Lepidoptera: Gelechiidae) to Bt cotton. Journal of Economic Entomology, 98, 947 954.
13. Carrière, Y., Ellers-Kirk, C., Biggs, R., Higginson, D.M., Dennehy, T.J. Tabashnik, B.E. (2004) Effects of gossypol on fitness costs associated with resistance to Bt cotton in pink bollworm. Journal of Economic Entomology, 97, 1710 1718.
14. Carrière, Y., Ellers-Kirk, C., Kamlesh, K., Heuberger, S., Whitlow, M., Antilla, L., Dennehy, T.J. Tabashnik, B.E. (2005a) Long-term evaluation of compliance with refuge requirements for Bt cotton. Pest Science Management, 61, 327 330.
15. Carrière, Y., Ellers-Kirk, C., Liu, Y.-B., Sims, M.A., Patin, A.L., Whitlow, M., Dennehy, T.J. Tabashnik, B.E. (2001) Fitness costs and maternal effects associated with resistance to transgenic cotton in the pink bollworm (Lepidoptera: Gelechiidae). Journal of Economic Entomology, 94, 1571 1576.
16. Carrière, Y., Ellers-Kirk, C., Sisterson, M., Antilla, L., Dennehy, T.J. Tabashnik, B.E. (2003) Long-term regional suppression of pink bollworm by Bacillus thuringiensis cotton. Proceedings of the National Academy of Sciences USA, 100, 1519 1523.
17. Carrière, Y. Tabashnik, B.E. (2001) Reversing insect adaptation to transgenic insecticidal plants. Proceedings of the Royal Society, Series B, Biological Sciences, 268, 1475 1480.
18. Cattaneo, M.G., Yafuso, C., Schmidt, C., Huang, C.-y., Rahman, M., Olson, C., Ellers-Kirk, C., Orr, B.J., Marsh, S.E., Antilla, L., Dutilleul, P. Carrière, Y. (2006) Farm-scale evaluation of the impacts of transgenic cotton on biodiversity, pesticide use, and yield. Proceedings of the National Academy of Sciences USA, 103, 7571 7576.
19. Chattopadhyay, A., Bhatnagar, N.B. Bhatnagar, R. (2004) Bacterial insecticidal toxins. Critical Reviews in Microbiology, 30, 33 54.
20. Cory, J.S. Hoover, K. (2006) Plant-mediated effects in insect-pathogen interactions. Trends in Ecology and Evolution, 21, 278 286.
21. Dent, D. (2000) Insect Pest Management. CABI Publishing, Wallingford.
22. Ferré, J. van Rie, J. (2002) Biochemistry and genetics of insect resistance to Bacillus thuringiensis. Annual Review of Entomology, 47, 501 533.
23. Forst, S. Nealson, K. (1996) Molecular biology of the symbiotic-pathogenic bacteria Xenorhabdus spp. and Photorhabdus spp. Microbiological Reviews, 60, 21 43.
24. Gassmann, A.J. Futuyma, D.J. (2005) Consequence of herbivory for the fitness cost of herbicide resistance: photosynthetic variation in the context of plant-herbivore interactions. Journal of Evolutionary Biology, 18, 447 454.
25. Gassmann, A.J., Stock, S.P., Carrière, Y. Tabashnik, B.E. (2006) Effect of entomopathogenic nematodes on the fitness cost of resistance to Bt toxin Cry1Ac in pink bollworm (Lepidoptera: Gelechiidae). Journal of Economic Entomology, 99, 920 926.
26. Ghalambor, C.K., Reznick, D.N. Walker, J.A. (2004) Constraints on adaptive evolution: the functional trade-off between reproduction and fast-start swimming performance in the Trinidadian guppy (Poecilia reticulata). American Naturalist, 164, 38 50.
27. Gouge, D.H., Smith, K.A., Lee, L.L. Henneberry, T.J. (1998) Control of pink bollworm Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae) with entomopathogenic nematodes (Rhabditida: Steinernematidae) and gossyplure in cotton. Recent Research Developments in Entomology, 2, 55 85.
28. Gould, F. (1998) Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annual Review of Entomology, 43, 701 726.
29. Gould, F., Anderson, A., Jones, A., Sumerford, D., Heckel, D.G., Lopez, J., Micinski, S., Leonard, R. Laster, M. (1997) Initial frequency of alleles for resistance to Bacillus thuringiensis toxins in field populations of Heliothis virescens. Proceedings of the National Academy of Sciences USA, 94, 3519 3523.
30. Hare, J.D. (2002) Plant genetic variation in tritrophic interactions. Multitrophic Level Interactions (eds T. Tscharntke B.A. Hawkins pp. 8 43. Cambridge University Press, Cambridge.
31. Herdt, R.W. (2006) Biotechnology in agriculture. Annual Review of Environment and Resources, 31, 265 295.
32. James, C. (2006) Global Status of Commercialized Biotech/GM Crops: 2006. International Service for the Acquisition of Agri-biotech Applications, Ithaca.
33. Janmaat, A.F. Myers, J.H. (2003) Rapid evolution and the cost of resistance to Bacillus thuringiensis in greenhouse populations of cabbage loopers, Trichoplusia ni. Proceedings of the Royal Society, Series B, Biological Sciences, 270, 2263 2270.
34. Janmaat, A.F. Myers, J.H. (2005) The cost of resistance to Bacillus thuringiensis varies with the host plant of Trichoplusia ni. Proceedings of the Royal Society, Series B, Biological Sciences, 272, 1031 1038.
35. Journey, A.M. Ostlie, K.R. (2000) Biological control of the western corn rootworm (Coleoptera: Chrysomelidae) using the entomopathogenic nematode, Steinernema carpocapsae. Environmental Entomology, 29, 822 831.
36. Kaya, H.K. Stock, S.P. (1997) Techniques in insect nematology. Manual of Techniques in Insect Pathology (ed. L.A. Lacey pp. 281 324. Academic Press, San Diego.
37. Koppenhöfer, A.M., Wilson, M., Brown, I., Kaya, H.K. Gaugler, R. (2000) Biological control agents for white grubs (Coleoptera: Scarabaeidae) in anticipation of the establishment of the Japanese beetle in California. Journal of Economic Entomology, 93, 71 80.
38. Lacey, L.A. (1997) Bacteria: laboratory bioassays of bacteria against aquatic insects with emphasis on larvae of mosquitoes and black flies. Manual of Techniques in Insect Pathology (ed. L.A. Lacey pp. 79 88. Academic Press, San Diego.
39. Littell, R.C., Milliken, G.A., Stroup, W.W. Wolfinger, R.D. (1996) sas System for Linear Models. SAS Institute Inc., Cary, NC.
40. Morin, S., Biggs, R.W., Sisterson, M.S., Shriver, L., Ellers-Kirk, C., Higginson, D., Holley, D., Gahan, L.J., Heckel, D.G., Carrière, Y., Dennehy, T.J., Brown, J.K. Tabashnik, B.E. (2003) Three cadherin alleles associated with resistance to Bacillus thuringiensis in pink bollworm. Proceedings of the National Academy of Sciences USA, 100, 5004 5009.
41. Morin, S., Henderson, S., Fabrick, J.A., Carrière, Y., Dennehy, T.J., Brown, J.K. Tabashnik, B.E. (2004) DNA-based detection of Bt resistance alleles in pink bollworm. Insect Biochemistry and Molecular Biology, 34, 1225 1233.
42. Ode, P.J. (2006) Plant chemistry and natural enemy fitness: effects on herbivore and natural enemy interactions. Annual Review of Entomology, 51, 163 185.
43. Park, Y. Stanley, D. (2006) The entomopathogenic bacterium, Xenorhabdus nematophila, impairs hemocytic immunity by inhibition of eicosanoid biosynthesis in adult crickets, Gryllus firmus. Biological Control, 38, 247 253.
44. Pittendrigh, B.R., Gaffney, P.J., Huesing, J.E., Onstad, D.W., Roush, R.T. Murdock, L.L. (2004) 'Active' refuges can inhibit the evolution of resistance in insects towards transgenic insect-resistant plants. Journal of Theoretical Biology, 231, 461 474.
45. Quinn, G.P. Keough, M.J. (2002) Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge.
46. Raymond, B., Sayyed, A.H., Hails, R.S. Wright, D.J. (2007) Exploiting pathogens and their impact on fitness costs to manage the evolution of resistance to Bacillus thuringiensis. Journal of Applied Ecology, 44, 768 780.
47. SAS Institute Inc 1999) sas/stat User's Guide, version 8. SAS Institute Inc., Cary, NC.
48. Shelton, A.M., Tang, J.D., Roush, R.T., Metz, T.D. Earle, E.D. (2000) Field tests on managing resistance to Bt-engineered plants. Nature Biotechnology, 18, 339 342.
49. Sisterson, M.S., Antilla, L., Carrière, Y., Ellers-Kirk, C. Tabashnik, B.E. (2004) Effects of insect population size on evolution of resistance to transgenic crops. Journal of Economic Entomology, 97, 1413 1424.
50. Sisterson, M.S., Carrière, Y., Dennehy, T.J. Tabashnik, B.E. (2005) Evolution of resistance to transgenic Bt crops: interactions between insect movement and field distribution. Journal of Economic Entomology, 98, 1751 1762.
51. Sokal, R.R. Rohlf, F.J. (1995) Biometry, 3rd edn. W.H. Freeman, New York.
52. Tabashnik, B.E. (1994) Evolution of resistance to Bacillus thuringiensis. Annual Review of Entomology, 39, 47 79.
53. Tabashnik, B.E., Biggs, R.W., Higginson, D.M., Henderson, S., Unnithan, D.C., Unnithan, G.C., Ellers-Kirk, C., Sisterson, M.S., Dennehy, T.J., Carrière, Y. Morin, S. (2005) Association between resistance to Bt cotton and cadherin genotype in pink bollworm. Journal of Economic Entomology, 98, 635 644.
54. Tabashnik, B.E., Cushing, N.L., Finson, N. Johnson, M.W. (1990) Field development of resistance to Bacillus thuringiensis in diamondback moth (Lepidoptera: Plutellidae). Journal of Economic Entomology, 83, 1671 1676.
55. Tabashnik, B.E., Dennehy, T.J. Carrière, Y. (2005) Delayed resistance to transgenic cotton in pink bollworm. Proceedings of the National Academy of Sciences USA, 102, 15389 15393.
56. Tabashnik, B.E., Gassmann, A.J., Crowder, D.W. Carrière, Y. (2008) Insect resistance to Bt crops: evidence versus theory. Nature Biotechnology, 26, 199 202.
57. Tabashnik, B.E., Gould, F. Carrière, Y. (2004) Delaying evolution of insect resistance to transgenic crops by decreasing dominance and heritability. Journal of Evolutionary Biology, 17, 904 912.