Transgenic insecticidal crops and natural enemies: A detailed review of laboratory studies

Environmental Entomology

Volumn 38, Issue 2, 2009, Pages 293-306

  Lövei, Gabor L ^a   Andow, David A ^b   Arpaia, Salvatore ^c  

^a DANISH INSTITUTE OF AGRICULTURAL SCIENCES   (Denmark)

^b UNIVERSITY OF MINNESOTA   (United States)

^c Trisaia Research Center   (Italy)

Author keywords

Biosafety; Laboratory experiments; Natural enemies; Review; Transgenic plants

Indexed keywords

BACTERIAL PROTEIN; ENDOTOXIN; HEMOLYSIN; INSECTICIDAL CRYSTAL PROTEIN, BACILLUS THURINGIENSIS; INSECTICIDE;

BIOPESTICIDE; BIOSAFETY; GENETICALLY MODIFIED ORGANISM; INHIBITOR; INSECT; LABORATORY METHOD; LITERATURE REVIEW; META-ANALYSIS; NATURAL ENEMY; PARASITOID; TOXIN;

ANIMAL; ARTHROPOD; ARTICLE; CROP; FACTUAL DATABASE; GENETICS; GROWTH, DEVELOPMENT AND AGING; INSECT CONTROL; LARVA; METHODOLOGY; SPECIES DIFFERENCE; TRANSGENIC PLANT;

ANIMALS; ARTHROPODS; BACTERIAL PROTEINS; CROPS, AGRICULTURAL; DATABASES, FACTUAL; ENDOTOXINS; HEMOLYSIN PROTEINS; INSECT CONTROL; INSECTICIDES; LARVA; PLANTS, GENETICALLY MODIFIED; SPECIES SPECIFICITY;

ARTHROPODA; CHRYSOPERLA; CHRYSOPIDAE;

EID: 65249086835     PISSN: 0046225X     EISSN: None     Source Type: Journal    
DOI: 10.1603/022.038.0201     Document Type: Article

References (105)

1. Ahmad, A., G. E. Wilde, R. J. Whitworth, and G. Zolnerowich. 2006. Effect of corn hybrids expressing the Coleopteran-specific Cry3Bbl protein for corn rootworm control on aboveground insect predators. J. Econ. Entomol. 99: 1085-1091.
2. AI Deeb, M. A., G. E. Wilde, and R. A. Higgins. 2001. No effect of Bacillus thuringensis corn and Bacillus thuringiensis on the predator Onus insidiosus (Hemiptera : Anthocoridae): Environ. Entomol. 30: 625-629.
3. Alvarez-Alfageme, F., M. Martinez, S. Pascual-Ruiz, P. Castanera, I. Diaz, and F. Ortego. 2007. Effects of potato plants expressing a barley cystatin on the predatory bug Podisus maculiventris via herbivorour prey feeding on the plant. Transg. Res. 16: 1-13.
4. Andow,D.A.,G. L. Lövei,and S. Arpaia. 2006. Bt transgenic crops, natural enemies and implications for environmental risk assessment. Nat. Biotechnol. 24: 749-751.
5. Armer,C. A.,R. E. Berry, and M. Kogan. 2000. Longevity of phytophagous heteropteran predators feeding on transgenic Bt-potato plants: Entomol. Exp. Appl. 95: 329-333.
6. Ashouri, A. S. Overney, D. Michaud, and C. Cloutier. 1998. Fitness and feeding are affected in the two-spotted stinkbug, Perillus bioculatus, by the cysteine proteinase inhibotor, oryzacystatin I. Arch. Insect Biochem. Physiol. 38: 74-83.
7. Ashouri, A., D. Michaud, and C. Cloutier. 2001. Recombinant and classically selected factors of potato plant resistance to the Colorado potato beetle, Leptinotarsa decemlineata, variously affect the potato aphid parasitoid Aphidius nigripes. BioControl 46: 401-412.
8. Bai, Y. Y., M. X. Jiang, and J. A. Cheng. 2005. Effects of transgenic crylAb rice pollen on fitness of Propylea japonica (Thunberg). J. Pest Sci. 78: 123-128.
9. Bai, Y. Y., M. X. Jiang, J. A. Cheng, and D. Wang. 2006. Effects of CrylAb toxin on Propylea japonica (Thunberg) (Coleoptera: Coccinellidae) through its prey, Nilaparvata lugens Stal (Homoptera: Delphacidae), feeding on transgenic Bt rice. Environ. Entomol. 35: 1130-1136.
10. Bauer, M. E., and D. J. Boethel. 2003. Effect of Bf-cotton expressing CrylA(c) on the survival and fecundity of two hymenopteran parasitoids (Braconidae, Encyrtidae) in the laboratory. Biol. Control 26: 325-332.
11. Bell, H. A., E. C. Fitches, R. E. Down, G. C. Marris, J. P. Edwards, J. A. Gatehouse, and A.M.R. Gatehouse. 1999. The effect of snowdrop lectin (GNA) delivered via artificial diet and transgenic plants on Eulophus pennicornis (Hymenoptera: Eulophidae), a parasitoid of the tomato moth Lacanobia oleracea (Lepidoptera : Noctuidae). J. Ins. Physiol. 45: 983-991.
12. Bell, H. A., E. C. Fitches, R. E. Down, L. Ford, G. C. Marris, J. P. Edwards, J. A. Gatehouse, and A.M.R. Gatehouse. 2001a. Effect of dietary cowpea trypsin inhibitor (CpTI) on the growth and development of the tomato moth Lacanobia oleracea (Lepidoptera: Noctuidae) and on the success of the gregarious ectoparasitoid Eulophus pennicornis (Hymenoptera: Eulophidae). Pest Manag. Sci. 57: 57-65.
13. Bell, H. A., E. C. Fitches, G. C. Marris, J. Bell, J. P. Edwards, J. A. Gatehouse, and A.M.R. Gatehouse. 2001b. Transgenic GNA expressing potato plants augment the beneficial biocontrol of Lacanobia oleracea (Lepidoptera; Noctuidae. by the parasitoid Euhphus pennicomis (Hymenoptera; Eulophidae). Transgen. Res. 10: 35-42.
14. Bell, H. A., R. E. Down, E. C. Fitches, J. P. Edwards, and A.M.R. Gatehouse. 2003. Impact of genetically modified potato expressing plant-derived insect resistance genes on the predatory bug Podisus maculioentris (Heteroptera: Pentatomidae): Biocontr. Sci. Technol. 13: 729-741.
15. Bell, H. A., A. E. Kirkbride-Smith, G. C. Marris, J. P. Edwards, and A.M.R. Gatehouse. 2004. Oral toxicity and impact on fecundity of three insecticidal proteins on the gregarious ectoparasitoid Euhphus pennicornis (Hymenoptera: Eulophidae). Agric. Forest Entomol. 6: 215-222.
16. Benchekroun, A., D. Michaud, B. Nguyen-Quoc, S. Overney, Y. Desjardins, and S. Yelle. 1995. Production of active oryzacystatin I in transgenic potato plants. Plant Cell Rep. 14: 585-588.
17. Bernal, C. C., R. M. Aguda, and M. B. Cohen. 2002. Effect of rice lines transformed with Bacillus thuringiensis toxin genes on the brown planthopper and its predator Cyrtorhinus lividipennis: Entomol. Exp. Appl. 102: 21-28.
18. Bernal, J. S., J. G. Griset, and P. O. Gillogly. 2002. Impacts of developing on Bt maize-intoxicated hosts on fitness parameters of a stem borer parasitoid. J. Entomol. Sci. 37: 27-42.
19. Birch, A.N.E., I. E. Geoghegan, M.E.N. Majerus, J. W. Mc- Nicol, C. A. Hackett, A.M.R. Gatehouse, and J. A. Gatehouse. 1999. Tri-trophic interactions involving pest aphids, predatory 2-spot ladybirds and transgenic potatoes expressing snowdrop lectin for aphid resistance. Mol. Breed. 5: 75-83.
20. Bouchard, E., C. Cloutier, and D. Michaud. 2003a. Oryzacystatin I expressed in transgenic potato induces digestive compensation in an insect natural predator via its herbivorous prey feeding on the plant. Mol. Ecol. 12: 2439-2446.
21. Bouchard, E., D. Michaud, and C. Cloutier. 2003b. Molecular interactions between an insect predator and its herbivore prey on transgenic potato expressing a cysteine proteinase inhibitor from rice. Mol. Ecol. 12: 2429-2437.
22. Burgess, E.P.J., G. L. Lövei, L. A. Malone, I. W. Nielsen, H. S. Gatehouse, and J. T. Christeller. 2002. Prey-mediated effects of the protease inhibitor aprotinin on the predatory carabid beetle Nebria brevicollis. J. Ins. Physiol. 48: 1093-1101.
23. Christeller, J. T., E.P.J. Burgess, V. Mett, H. S. Gatehouse, N. P. Markwick, C. Murray, L. A. Malone, M. Wright, B. A. Philip, D. Watt, L. N. Gatehouse, G. L. Lövei, A. L. Shannon, M. M. Phung, L. Watson, and W. A. Laing. 2002. The expression of a mammalian proteinase inhibitor, bovine spleen trypsin inhibitor (SI), in tobacco and effects on Helicoverpa armigera larvae. Transgen. Res. 11: 161-173.
24. Crickmore, N., D. Zeigler, A. Bravo, E. Schnepf, D. Lereclus, J. Baum, J. Van Rie, and D. Dean. 2007. Bacillus thuringiensis toxin nomenclature. (http://www.lifesci. Sussex.ac.uk/Home/Neil-Crickmore/Bt, accessed 20 July 2007).
25. Couty, A., and G. M. Poppy. 2001. Does host-feeding on GNA-intoxicated aphids by Aphelinus abdominalis affect their longevity and/or fecundity? Entomol. Exp. Appl. 100: 331-337.
26. Couty, A., S.J. Clark, and G.M. Poppy. 2001a. Are fecundity and longevity of female Aphelinus abdominalis affected by development in GNA-dosed Macrosiphum euphorbias? Physiol. Entomol. 26: 287-293.
27. Couty, A., G. de la Vina, S. J. Clark, L. Kaiser, M. H. Pham- Delegue, and G. M. Poppy. 2001b. Direct and indirect sublethal effects of Galanthus nivalis agglutinin (GNA) on the development of a potato-aphid parasitoid, Aphelinus abdominalis (Hymenoptera: Aphelinidae). J. Ins. Physiol. 47: 553-561.
28. Couty, A., R. E. Down, A.M.R. Gatehouse, L. Kaiser, M. H. Pham-Delegue, and G. M. Poppy. 2001c. Effects of artificial diet containing GNA and GNA-expressing potatoes on the development of the aphid parasitoid Aphidius ervi Haliday (Hymenoptera: Aphidiidae). J. Ins. Physiol. 47: 1357-1366.
29. Davidson, M. M., R. C. Butler, S. D. Wratten, and A. J. Conner. 2006. Impacts of insect-resistant transgenic potatoes on the survival and fecundity of a parasitoid and an insect predator. Biol. Control 37: 224-230.
30. Dogan, E. B., R. E. Berry, G. L. Reed, and P. A. Rossignol. 1996. Biological parameters of convergent lady beetle (Coleoptera: Coccinellidae) feeding on aphids (Homoptera: Aphididae) on transgenic potato. J Econ. Entomol. 89: 1105-1108.
31. Down, R. E., L. Ford, S. D. Woodhouse, RJ.M. Raemaekers, B. Leitch, J. A. Gatehouse, and A.M.R. Gatehouse. 2000. Snowdrop lectin (GNA) has no acute toxic effects on a beneficial insect predator, the 2-spot ladybird (Adalia bipunctata L.). J. Insect Physiol. 46: 379-391.
32. Down, R. E., L. Ford, S. D. Woodhouse, G. M. Davison, M.E.N. Majerus, J. A. Gatehouse, and A.M.R. Gatehouse. 2003. Tritrophic interactions between transgenic potato expressing snowdrop lectin (GNA), an aphid pest (peach-potato aphid; Myzus persicae (Sulz.) and a beneficial predator, 2-spot ladybird (Adalia bipunctata L.). Transgen. Res. 12: 229-241.
33. Duan, J. J., G. Head, M. J. Mckee, T. E. Nickson, J. W. Martin, and F. S. Sayegh. 2002. Evaluation of dietary effects of transgenic corn pollen expressing Cry3Bbl protein on a non-target ladybird beetle, Coleomegilla maculate. Entomol. Exp. Appl. 104: 271-280.
34. Duan, J. J., M. S. Paradise, J. G. Lundgren, J. T. Bookout, C. J. Jiang,and R. N. Wiedenmann. 2006. Assessing nontarget impacts of Bt corn resistant to corn rootworms: tier-1 testing with larvae of Poecilus chalcites (Coleoptera: Carabidae). Environ. Entomol. 35: 135-142.
35. Dutton, A., H. Klein,J. Romeis,and F. Bigler. 2002. Uptake of Bt-toxin by herbivores feeding on transgenic maize and consequences for the predator Chrysoperla carnea. Ecol. Entomol. 27: 441-447.
36. [EC] European Council. 2001. Directive 2001/18/EC. Official J. Eur. Comm. L 106: 1-38.
37. [EFSA] European Food Safety Authority. 2006. Guidance document of the scientific panel on genetically modified organisms for the risk assessment of genetically modified plants and derived food and feed. EFSA J. 99: 1-100.
38. Felton, G. W., and J. A. Gatehouse. 1996. Antinutritive plant defence mechanisms, pp. 373-416. In M. J. Lehane and P. F. Billingsley (eds.), Biology of the insect midgut. Chapman & Hall, London, United Kingdom.
39. Ferry, N., R. J.M. Raemaekers, M. E.N. Majerus, L. Jouanin, G. Port, J. A. Gatehouse, and A. M.R. Gatehouse. 2003. Impact of oilseed rape expressing the insecticidal cysteine protease inhibitor oryzacystatin on the beneficial predator Harmonia axyridis (multicoloured Asian ladybeetle). Mol. Ecol. 12: 493-504.
40. Geng, J.-H., Z.-R. Shen, K. Song, and L. Zheng. 2006. Effect of pollen of regular cotton and transgenic Bt+CpTI cotton on the survival and reproduction of the parasitoid wasp Trichogrammachilonis (Hymenoptera: Trichogrammatidae) in the laboratory. Environ. Entomol. 35: 1661-1668.
41. Gonzalez-Zamora, J. E., S. Camunez, and C. Avilla. 2007. Effects of Bacillus thuringiensis Cry toxins on development and reproductive characteristics of the predator Orius alhidipennis (Hemiptera: Anthocoridae) under laboratory conditions. Environ. Entomol. 36: 1246-1253.
42. Griffiths, J. S., S. M. Haslam, T. L. Yang, S. F. Garczynski, B. Mulloy, H. Morris, P. S. Cremer, A. Dell, M. J. Adang, and R. V. Aroian. 2005. Glycolipids as receptors for Bacillus thuringiensis crystal toxin. Science 307: 922-925.
43. Haider, M. Z., B. H. Knowles, and D. J. Ellar. 1986. Specificity of Bacillus thuringiensis var. colmeri insecticidal δ-endotoxin is determined by differential proteolytic processing of the protoxin by larval gut proteases. Eur. J. Biochem. 156: 531-540.
44. Harwood, J. D., R. A. Samson, and J. J. Obrycki. 2006. No evidence for the uptake of Cryl Ab Bt-endotoxins by the generalist predator Scarites subterraneus (Coleoptera: Carabidae) in laboratory and field experiments. Biocont. Sci. Technol. 16: 377-388.
45. Hilbeck, A., M. Baumgartner, P. M. Fried, and F. Bigler. 1998a. Effects of transgenic Bacillus thuringiensis cornfed prey on mortality and development time of immature Chrysoperlacarnea (Neuroptera: Chrysopidae). Environ. Entomol. 27: 480-487.
46. Hilbeck, A., W. J. Moar, M. Pusztai-Carey, A. Filippini, and F. Bigler. 1998b. Toxicity of Bacillus thuringiensis CrylAb toxin to the predator Chrysoperla carnea (Neuroptera: Chrysopidae). Environ. Entomol. 27:1255-1263.
47. Hilbeck, A., W. J. Moar, M. Pusztai-Carey, A. Filippini, and F. Bigler. 1999. Prey-mediated effects of CrylAb toxin and protoxin and Cry2A protoxin on the predator Chrysoperla carnea. Entomol. Exp. Appl. 91: 305-316.
48. Hilder, V. A., K. S. Powell, A. M.R. Gatehouse, J. A. Gatehouse, L. N. Gatehouse, Y. Shi, W. D.O. Hamilton, A. Merryweather, C. A. Newell, J. C. Timans, W. J. Peumans, E. Vandamme, and D. Boulter. 1995. Expression of snowdrop lectin in transgenic tobacco plants results in added protection against aphids. Transgen. Res. 4: 18-25.
49. Hogervorst, P. A.M., N. Ferry, A. M.R. Gatehouse, F. L. Waeckers, and J. Romeis. 2006. Direct effects of snowdrop lectin (GNA) on larvae of three aphid predators and fate of GNA after ingestion. J. Ins. Physiol. 52: 614-624.
50. Johnson, M. T., F. Gould, and C. Kennedy. 1997. Effects of natural enemies on relative fitness of Heliothis virescens genotypes adapted and not adapted to resistant host plants. Entomol. Exp. Appl. 82: 219-231.
51. Jørgensen, H. B., and G. L. Lövei. 1999. Tri-trophic effect on predator feeding: consumption by the carabid Harpalus affinis of Heliothis armigera caterpillars fed on proteinase inhibitor-containing diet. Entomol. Exp. Appl. 93: 113-116.
52. Kalushkov, P., and I. Hodek. 2005. The effects of six species of aphids on some life history parameters of the ladybird Propylea quatuordedmpunctata (Coleoptera : Coccinellidae). Eur. J. Entomol. 102: 449-452.
53. Kalushkov, P., and O. J. Nedved. 2005. Genetically modified potatoes expressing Cry 3A protein do not affect aphidophagous coccinellids. J. Appl. Entomol. 129: 401-406.
54. Liu, X. X., C. G. Sun, and Q. W. Zhang. 2005a. Effects of transgenic CrylA+ CpTI cotton and CrylAc toxin on the parasitoid, Campoketis chlorideae (Hymenoptera:Ichneumonidae). Insect Sci. 12: 101-107.
55. Liu, X. X., Q. W. Zhang, J. Z. Zhao, Q. N. Cai, H. L. Xu, and J. C. Li. 2005b. Effects of the CrylAc toxin of Bacillus thuringiensis on Microplitis mediator, a parasitoid of the cotton bollworm, Helicoverpa armigera. Entomol. Exp. Appl. 114: 205-213.
56. Liu, X. X., Q. W. Zhang, J. Z. Zhao, J. C. Li, B. L. Xu, and X. M. Ma. 2005c. Effects of Bt transgenic cotton lines on the cotton bollworm parasitoid Microptilis mediator in the laboratory. Biol. Control 35: 134-141.
57. Lövei, G. L., and S. Arpaia. 2005. The impact of transgenic plants on natural enemies: a critical review of laboratory studies. Entomol. Exp. Appl. 114: 1-14.
58. Lozzia, G. C., C. Furlanis, B. Manachini, and I. E. Rigamonti. 1998. Effects of Bt corn on Bhopalosiphumpadi L. (Rhynchota Aphididae) and on its predator Chrysoperla camea Stephen (Neuroptera Chrysopidae). Boll. Zoool. Agr. Bachicol. 30: 153-164.
59. Ludy, C, and A. Lang. 2006. Bt maize pollen exposure and impact on the garden spider, Araneus diadematus. Entomol. Exp. Appl. 118: 145-156.
60. Lundgren, J. G., and R. N. Wiedenmann. 2002. Coleopteran-specific Cry3Bb toxin from transgenic com pollen does not affect the fitness of a nontarget species, Coleomegilla maculata DeGeer (Coleoptera : Coccinellidae): Environ. Entomol. 31: 1213-1218.
61. Lundgren, J. G., and R. W. Wiedenmann. 2004. Nutritional suitability of corn pollen for the predator Coleomegilla maculata (Coleoptera:Coccinellidae). J. Ins. Physiol. 50: 567-575.
62. Lundgren, J. G., and R. W. Wiedenmann. 2005. Tritrophic interactions among Bt (Cry3Bbl) com, aphid prey and the predator Coleomegilla maculata (Coleoptera: Coccinellidae). Environ. Entomol. 34: 1621-1625.
63. Malcolm, S. B. 1992. Prey defence and predator foraging, pp. 458-475. In M. J. Crawley (ed.), Natural enemies. Blackwell Scientific, Oxford, United Kingdom.
64. Marvier, M., C. McCreedy, J. Regetz, and P. Kareiva. 2007. A meta-analysis of effects of Bt cotton and maize on non-target invertebrates. Science 316: 1475-1477.
65. Meier, M. S., and A. Hilbeck. 2001. Influence of transgenic Bacillus thuringiensis corn-fed prey on prey preference of immature Chrysoperla camea (Neuroptera: Chrysopidae): Basic Appl. Ecol. 2: 35-44.
66. Meissle, M., E. Vojtech, and G. M. Poppy. 2005. Effects of Bt maize-fed prey on the generalist predator Poecilus cupreus L. (Coleoptera: Carabidae). Transgen. Res. 14:123-132.
67. Mizuki, E., Y. S. Park, H. Saitoh, S. Yamashita, T. Akao, K. Higuchi, and M. Ohba. 2000. Parasporin, a human leukemic cell-recognizing parasporal protein of Bacillus thuringiensis. Clin. Diagn. Lab. Immunol. 7: 625-634.
68. Mullin, C. A., M. C. Saunders, I. I.T. W. Leslie, D. J. Biddinger, and S. J. Fleischer. 2005. Toxic and behavioral effects to Carabidae of seed treatments used on Cry3Bbl- and CrylAb/c-protected corn. Environ. Entomol. 34: 1626-1636.
69. National Research Council. 2002. Environmental effects of transgenic plants. National Academy Press, Washington, DC.
70. O'Callaghan, M., T. R. Glare, E. P.J. Burgess, and L. A. Malone. 2005. Effects of plants genetically modified for insect resistance on nontarget organisms. Annu. Rev. Entomol. 50: 271-292.
71. Omolo, E. O., M. D. James, E. O. Osir, and J. A. Thomson. 1997. Cloning and expression of a Bacillus thuringiensis (Ll-2) gene encoding a crystal protein active against Glossina morsitans morsitans and Chilo partellus. Curr. Microbiol. 34: 118-121.
72. Pilcher, C. D., J. J. Obrycki, M. E. Rice, and L. C. Lewis. 1997. Preimaginal development, survival, and field abundance of insect predators on transgenic Bacillus thuringiensis corn: Environ. Entomol. 26: 446-454.
73. Ponsard, S., A. P. Gutierrez, and N. J. Mills. 2002. Effect of Bt-toxin (CrylAc) in transgenic cotton on the adult longevity of four heteropteran predators. Environ. Entomol. 31: 1197-1205.
74. Pruetz, G., and K. Dettner. 2004. Effect of Bt corn leaf suspension on food consumption by Chilo partellus and life history parameters of its parasitoids Cotesia flavipes under laboratory conditions. Entomol. Exp. Appl. III: 179-187.
75. Pruetz, G., A. Brink, and K. Dettner. 2004. Transgenic insect-resistant corn affects the fourth trophic level: effects of the Bacillus thuringiensis-corn on the facultative hyperparasitoid Tetrastichus howardi. Naturwissenschaften 91: 451-454.
76. Ramirez-Romero, R., J. S. Bernal, J. Chaufaux, and L. Kaiser. 2007. Impact assessment of Bt-maize on a moth parasitoid, Cotesia marginiventris (Hymenoptera: Braconidae), via host exposure to purified Cryl Ab protein or Bt-plants. Crop Prot. 26: 953-962.
77. Riddick, E. W., and P. Barbosa. 1998. Impact of Cry3A- intoxicated Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) and pollen on consumption, development, and fecundity of Coleomegilla maculata (Coleoptera: Coccinellidae). Ann. Entomol. Soc. Am. 91: 303-307.
78. Riddick, E. W., and P. Barbosa. 2000. Cry3A-intoxicated Leptinotarsa decemlineata (Say) are palatable prey for Lebia grandis Hentz. J. Entomol. Sci. 35: 342-346.
79. Rodrigo-Simon, A., R. A. de Maagd, C. Avilla, P. L. Bakker, J. Molthoff, J. E. Gonzalez-Zamora, and J. Ferre. 2006. Lack of detrimental effects of Bacillus thuringiensis Cry toxins on the insect predator Chrysoperla carnea: a toxicological, histopathological, and biochemical analysis. Appl. Environ. Microbiol. 72: 1595-1608.
80. Romeis, J., D. Babendreier, and F. L. Wackers. 2003. Consumption of snowdrop lectin (Galanthus nivalis agglutinin) causes direct effects on adult parasitic wasps. Oecologia (Berl.) 134: 528-536.
81. Romeis, J., A. Dutton, and F. Bigler. 2004. Bacillus thuringiensis toxin (CrylAb) has no direct effect on larvae of the green lacewing Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae). J. Ins. Physiol. 50: 175-183.
82. Romeis, J., M. Meissle, and F. Bigler. 2006. Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nat. Biotechnol. 24: 63-71.
83. Rovenska, G. Z., R. Zemek, J.E.U. Schmidt, and A. Hilbeck. 2005. Altered host plant preference of Tetranychus urticae and prey preference of its predator Phytoseiulus persimilis (Acari : Tetranychidae, Phytoseiidae) on transgenic Cry3Bb-eggplants. Biol. Control 33: 293-300.
84. Sanders, C. J., J. K. Pell, G. M. Poppy, A. Raybould, M. Garcia-Alonso, and T. H. Schuler. 2007. Host-plant mediated effects of transgenic maize on the insect parasitoid Campoletis sonorensis (Hymenoptera: Ichneumonidae). Biol. Control 40: 362-369.
85. Schuler, T. H., I. Denholm, L. Jouanin, S. J. Clark, A. J. Clark, and G. M. Poppy. 2001. Population-scale laboratory studies of the effect of transgenic plants on nontarget insects. Mol. Ecol. 10: 1845-1853.
86. Schuler, T. H., R.P.J. Potting, I. Denholm, S. J. Clark, A. J. Clark, C. N. Stewart, and G. M. Poppy. 2003. Tritrophic choice experiments with Bt plants, the diamondback moth (Plutella xylostella) and the parasitoid Cotesia plutellae. Transgen. Res. 12: 351-361.
87. Schuler, T. H., I. Denholm, S. J. Clark, C. N. Stewart, and G. M. Poppy. 2004. Effects of Bt plants on the development and survival of the parasitoid Cotesia plutellae (Hymenoptera: Braconidae) in susceptible and Bt-resistant larvae of the diamondback moth, Plutella xyhstella (Lepidoptera : Plutellidae). J. Ins. Physiol. 50: 435-443.
88. Schuler, T. H., A. J. Clark, S. J. Clark, G. M. Poppy, C. N. Stewart, and I. Denholm. 2005. Laboratory studies of the effects of reduced prey choice caused by Bt plants on a predatory insect. Bull. Entomol. Res. 95: 243-247.
89. Setamou, M., J. S. Bernal, J. C. Legaspi, and T. E. Mirkov. 2002a. Parasitism and location of sugarcane borer (Lepidoptera: Pyralidae) by Cotesia flavipes (Hymenoptera: Braconidae) on transgenic and conventional sugarcane. Environ. Entomol. 31: 1219-1225.
90. Setamou, M., J. S. Bernal, J. C. Legaspi, and T. E. Mirkov. 2002b. Effects of snowdrop lectin (Galanthus nivalis agglutinin) on fitness of Cotesia flavipes (Hymenoptera : Braconidae), a parasitoid of the nontarget pest Diaeterella saccharalis (Lepidoptera: Crambidae). Ann. Entomol. Soc. Am. 95: 75-83.
91. Sharma, H. C, R. Arora, and G. Pampapathy. 2007. Influence of transgenic cottons with Bacillus thuringiensis CrylAc gene on the natural enemies of Helicoverpa armigera. BioControl 52: 469-489.
92. Sokal, R. R., and F. J. Rohlf. 1995. Biometry, 3rd ed. Freeman, San Francisco, CA.
93. Sterk, G., S. A. Hassan, M. Baillod, F. Bakker, F. Bigler, S. Blumel, H. Bogenschutz, E. Boiler, B. Bromand, J. Brun, J.N.M. Calis, J. Coremans-Pelseneer, C. Duso, A. Garrido, A. Grove, U. Heimbach, H. Hokkanen, J. Jacas, G. Lewis, L. Moreth, L. Polgar, L. Roversti, L. Samsoe Peterson, B. Sauphanor, L. Schaub, A. Staubli, J. J. Tuset, A. Vainio, M. Van Veire, G. Viggiani, E. Vinuela, and H. Vogt. 1999. Results of the seventh joint pesticide testing programme carried out by the IOBC/WPRS-Working Group 'Pesticides and Beneficial Organisms'. BioControl 44: 99-117.
94. Tomov. B.W., and J.S. Bernal. 2003. Effects of GNA transgenic sugarcane on life history parameters of Parallorhogaspyralophagus (Marsh) (Hymenoptera: Braconidae), a parasitoid of Mexican rice borer. J. Econ. Entomol. 96: 570-576.
95. Tomov, B. W., J. S. Bernal, and S. B. Vinson. 2003. Impacts of transgenic sugarcane expressing GNA lectin on parasitism of Mexican rice borer by Parallorhogas pyralophagus (Marsh) (Hymenoptera: Braconidae). Environ. Entomol. 32: 866-872.
96. Tufte, E. W. 1997. Visual explanations. Graphics Press, Cheshire, CT.
97. Turlings, T.C.J., P. M. Jeanbourquin, M. Held, and T. Degen. 2005. Evaluating the induced-odour emission of a Bt maize and its attractiveness to parasitic wasps. Transgen. Res. 14: 807-816.
98. van Frankenhuyzen, K., and C. Nystrom. 2002. The Bacillus thuringiensis toxin specificity database. (http://www.glfc.cfs.nrcan.gc.can/ bacillus).
99. Vaupel, J. W., and A. I. Yashin. 1985. Heterogeneity's ruses: some surpsiring effects of selection on population dynamics. Am. Stat. 39: 176-185.
100. Vojtech, E., M. Meissle, and G. M. Poppy. 2005. GM effects of Bt maize on the herbivore Spodoptera littoralis (Lepidoptera: Noctuidae) and the parasitoid Cotesia marginiventris (Hymenoptera: Braconidae). Transgen. Res. 14: 133-144.
101. Wang, Z.-Y.,Y. Wu,K.-L. He, and S.-X.Bai. 2007. Effects of transgenic Bt maize pollen on longevity and fecundity of Trichogramma ostriniae in laboratory conditions. Bull. Insectol. 60: 49-55.
102. Zhang, G. F., F. H. Wan, W. X. Liu, and H. Y. Guo. 2006a. Early instar response to plant-delivered Bt-toxin in a herbivore (Spodoptera litura) and a predator (Propylaea japonica). Crop Prot. 25: 527-533.
103. Zhang, G. F, F. H. Wan, G. L. Lovei, W. X. Liu, and J. Y. Guo. 2006. Transmission of Bt toxin to the predator Propylaea japonica (Coleoptera: Coccinellidae) through its aphid prey feeding on transgenic Bt cotton. Environ. Entomol. 35: 143-150.
104. Zwahlen, C, W. Nentwig, F. Bigler, and A. Hilbeck. 2000. Tritrophic interactions of transgenic Bacillus thuringiensis corn, Anaphothrips obscurus (Thysanoptera: Thripidae), and the predator Orius majusculus (Heteroptera : Anthocoridae): Environ. Entomol. 29: 846-850.
105. Received 7 September 2007; accepted 11 November 2008.