Impact of transgenic VIP3A x Cry1Ab lepidopteran-resistant field corn on the nontarget arthropod community

Environmental Entomology

Volumn 34, Issue 5, 2005, Pages 1267-1291

  Dively, Galen P ^a  

^a Bldg 142   (United States)

Author keywords

Bacillus thuringiensis corn; Cry1Ab; Nontarget effects; Principal response curves; VIP3A

Indexed keywords

ARTHROPOD; BIOINDICATOR; COMMUNITY COMPOSITION; NONTARGET ORGANISM; SPECIES DIVERSITY; TRANSGENIC PLANT;

ARTHROPODA; BACILLUS THURINGIENSIS; HEXAPODA; INSECTA; LEPIDOPTERA; ZEA MAYS;

EID: 26444521718     PISSN: 0046225X     EISSN: None     Source Type: Journal    
DOI: 10.1093/ee/34.5.1267     Document Type: Article

References (118)

1. Al-deeb, M. A., G. E. Wilde, J. M. Blair, and T. C. Todd. 2003. Effect of Bt corn for corn rootworm control on nontarget soil microarthropods and nematodes. Environ. Entomol. 32: 859-865.
2. Armer, C. A., R. N. Wiedenmann, and D. R. Bush. 1996. Plant feeding site selection on soybean by the facultatively phytophagous predator Orius insidiosus. Entomol. Exp. Appl. 86: 109-118.
3. Benrey, B., and R. F. Denno. 1997. The slow growth-high mortality hypothesis: a test using the cabbage butterfly. Ecology. 78: 987-999.
4. Benton, A. H., and A. J. Crump. 1981. Observations on the spring and summer behavior of the 12-spotted ladybird beetle, Coleomegilla maculata (Degeer) (Coleoptera: Coccinellidae). J.N.Y. Entomol. Soc. 89: 102-108.
5. Bitzer, R. J., M. E. Rice, C. D. Pilcher, C. Pilcher, and W-K.F. Lam. 2005. Biodiversity and community structure of soil-dwelling springtails (Entognatha: Collembola) in transgenic rootworm Bt corn. Environ. Entomol. 34: 1346-1376.
6. Bhatti, M. A., J. Duan, G. Head, C. Jiang, M. J. McKee, T. E. Nickson, C. L. Pilcher, and C. D. Pilcher. 2005. Field evaluation of the impact of corn rootworm (Coleoptera: Chrysomelidae) protected Bt corn on ground-dwelling invertebrates. Environ. Entomol. 34: 1325-1335.
7. Boo, K. S., I. B. Chung, K. S. Han, J. A. Pickett, and L. J. Wadhams. 1998. Response of the lacewing Chrysopa cognata Wesmael (Neuroptera: Chrysopidae) to pheromones of its aphid (Homoptera: Aphididae) prey. J. Chem. Ecol. 24: 631-643.
8. Bourguet, D., J. Chaufaux, A. Micoud, M. Delos, B. Naibo, F. Bombarde, G. Marque, N. Eychenne, and C. Pagliari. 2002. Ostrinia nubilalis parasitism and the field abundance of non-target insects in transgenic Bacillus thuringiensis corn (Zea mays). Environ. Biosafety Res. 1: 49-60.
9. Brust, G. E. 1991. A method for observing below-ground pest-predator interactions in corn agroecosystems. J. Entomol. Sci. 26: 1-8.
10. Brust, G. E., B. R. Stinner, and D. McCartney. 1986. Predator activity and predation in corn agroecosystems. Environ. Entomol. 15: 1017-1021.
11. Canard, M., Y. Semeria, and T. R. New. 1984. Biology of Chrysopidae. Dr. W. Junk Publishers, The Hague, The Netherlands.
12. Candolfi, M., K. Brown, B. Reber, and H. Schmidli. 2003. A faunistic approach to assess potential side effects of genetically modified Bt corn on nontarget arthropods under field conditions. Biocontrol Sci. Technol. 14: 129-170.
13. Clancy, K. M., and P. W. Price. 1987. Rapid herbivore growth enhances enemy attack: sublethal plant defenses remain a paradox. Ecology. 68: 736-738.
14. Clark, M. S., J. M. Luna, N. D. Stone, and R. R. Youngman. 1993. Habitat preferences of generalist predators in reduced-tillage corn. J. Entomol. Sci. 28: 404-416.
15. Clark, M. S., J. M. Luna, N. D. Stone, and R. R. Youngman. 1994. Generalist predator consumption of armyworm (Lepidoptera: Noctuidae) and effect of predator removal on damage in no-till corn. Environ. Entomol. 23: 617-622.
16. Coderre, D. 1987. Effectiveness of aphidophagous insects on maize, pp. 211-214. In Niemczy, E., and A.F.G. Dixon (eds.), Ecology and effectiveness of aphidophaga. SPB Academic Publishing, The Hague, The Netherlands.
17. Coll, M. 1996. Feeding and ovipositing on plants by an omnivorous insect predator. Oecologia (Berl.). 105: 214-220.
18. Coll, M., and D. G. Bottrell. 1991. Microhabitat and resource selection of the European corn borer (Lepidoptera: Pyralidae) and its natural enemies in Maryland field corn. Environ. Entomol. 20: 526-533.
19. Coll, M., and D. G. Bottrell. 1992. Mortality of European corn borer larvae by natural enemies in different corn microhabitats. Biol. Control. 2: 95-103.
20. Crecchio, C., and G. Stotzky. 1998. Insecticidal activity and biodegradation of the toxin from Bacillus thuringiensis subsp. kurstaki bound to humic acids from soil. Soil Biol. Biochem. 30: 463-470.
21. Croft, B. A. 1990. Arthropod biological control agents and pesticides. Wiley, New York.
22. Cuppen, J.G.M., P. J. Van den Brink, K. F. Uil, E. Camps, and T.C.M. Brock. 2000. Impact of the fungicide carbendazim in freshwater microcosms. II Water quality, breakdown of particulate organic matter and responses of macro-invertebrates. Aquatic Toxicol. 48: 233-250.
23. Czarnecki, A., and J. Losinski. 1995. The effect of GT seed dressing on the community of Collembola in soil under sugar beet. Pedobiologia. 28: 427-31.
24. Daly, T., and G. D. Buntin. 2005. Effect of Bacillus thuringiensis transgenic corn for lepidopteran control on non-target arthropods. Environ. Entomol. 34: 1292-1301.
25. De Moraes, C. M., W. J. Lewis, P. W. Paré, H. T. Alborn, and J. H. Tumlinson. 1998. Herbivore-infested plants selectively attract parasitoids. Nature (Lond.). 393: 570-573.
26. Dicke, F. F., and J. L. Jarvis. 1962. The habits and seasonal abundance of Orius insidiosus (Say) (Hemiptera-Heteroptera: Anthocoridae) on corn. J. Kansas Entomol. Soc. 35: 339-344.
27. Dively, G. P., and R. Rose. 2003. Effects of Bt transgenic and conventional insecticide control on the non-target natural enemy community in sweet corn, pp. 265-274. In R. G. Van Driesche (ed.), Proceedings of the First International Symposium on Biological Control of Arthropods. U.S. Dep. Agric. Forest Service, Morgantown, WV.
28. Dively, G. P., R. Rose, M. K. Sears, R. L. Hellmich, D. E. Stanley-Horn, D. D. Calvin, J. M. Russo, and P. L. Anderson. 2004. Effects on monarch butterfly larvae (Lepidoptera: Danaidae) after continuous exposure to Crylab-expressing corn during anthesis. Environ. Entomol. 33: 1116-1125.
29. 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.
30. Donegan, K. K., C. J. Palm, V. J. Fieland, L. A. Porteous, L. M. Ganio, D. L. Schaller, and R. J. Seidler. 1995. Changes in levels, species and DNA fingerprints of soil microorganisms associated with cotton expressing the Bacillus thuringiensis var. kurstaki endotoxin. Appl. Soil Ecol. 2: 111-124.
31. Donegan, K. K., D. L. Schaller, J. K. Stone, L. M. Ganio, G. Reed, P. B. Hamm, and R. J. Seidler. 1996. Microbial populations, fungal species diversity and plant pathogen levels in field plots of potato plants expressing the Bacillus thuringiensis var. tenebrionis endotoxin. Transgenic Res. 5: 25-35.
32. Drukker, B., J. Bruin, and M. Sabelis. 2000. Anthocorid predators learn to associate herbivore induced plant volatiles with presence or absence of prey. Physiol. Entomol. 25: 260-265.
33. Duelli, P. 1984. Flight, dispersal, migration, pp. 129-133. In M. Canard, Y. Semeria, and T. R. New (eds.), Biology of Chrysopidae. Dr. W. Junk Publishers, The Hague, The Netherlands.
34. 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.
35. Estruch, J. J., G. W. Warren, M. A. Mullins, G. J. Nye, J. A. Craig, and M. G. Koziel. 1996. Vip3A, a novel Bacillus thuringiensis vegetative insecticidal protein with a wide spectrum of activities against lepidopteran insects. Proc. Natl. Acad. Sci. U.S.A. 93: 5389-5394.
36. Fitt, G., and L. Wilson. 2003. Non-target effects of Bt cotton: a case study from Australia, pp. 183-190. In R. J. Akhurst, C. E. Beard, and P. Hughes (eds.), Biotechnology of Bacillus thuringiensis and its environmental impact. CSIRO, Canberra, Australia.
37. Frampton, G. K., S. D. Langton, P. W. Greig-Smith, and A. R. Hardy. 1992. Changes in the soil fauna at Boxworth, pp. 132-143. In P. Greig-Smith, G. K. Frampton, and T. Hardy (eds.), Pesticides, cereal farming and the environment: the Boxworth project. HMSO, London, UK.
38. Godfray, H.C.J. 1994. Parasitoids, behavioral and evolutionary ecology. Princeton University Press, Princeton, NJ.
39. Groot, A. T., and M. Dicke. 2002. Insect-resistant transgenic plants in a multi-trophic context. Plant J. 31: 387-406.
40. Hagen, K. S. 1987. Nutritional ecology of terrestrial insect predators, pp. 533-577. In F. Slansky and J. G. Rodriguez (eds.), Nutritional ecology of insects, mites, spiders, and related invertebrates. Wiley, New York.
41. Head, G., J. B. Surber, J. A. Watson, J. W. Martin, and J. J. Duan. 2002. No detection of Cry1Ac protein in soil after multiple years of transgenic Bt cotton (Bollgard®) use. Environ. Entomol. 31: 30-36.
42. Head, G., W. Moar, M. Eubanks, B. Freeman, J. Ruberson, A. Hagerty, and S. Turnipseed. 2005. A multiyear, large-scale comparison of arthropod populations on commercially managed Bt and non-Bt cotton fields. Environ. Entomol. 34: 1257-1266.
43. Heegaard, E., and V. Vandvik. 2004. Climate change affects the outcome of competitive interactions - an application of principal response curves. Oecologia (Berl.). 139: 459-466.
44. Hense, B. A., G. F. Severin, G. Welzl, and K. W. Schramm. 2004. Effects of 17α-ethinylestradiol on zoo- and phytoplankton in lentic microcosms. Anal. Bioanal. Chem. 378: 716-724.
45. Hilbeck, A., M. Baumgartner, M. P. Fried, and F. Bigler. 1998a. Effects of transgenic Bacillus thuringiensis cornfed prey on mortality and development time of immature Chrysoperla carnea (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 Cry1Ab 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 Cry1Ab toxin and protoxin and Cry2A protoxin on the predator Chrysoperla carnea. Entomol. Exp. Appl. 91: 305-316.
48. Hoffmann, M. P., M. S. Orfanedes, L. H. Pedersen, J. J. Kirkwyland, and E. R. Hoebeke. 1997. Survey of lady beetles (Coleoptera: Coccinellidae) in sweet corn using yellow sticky cards. J. Entomol. Sci. 32: 358-369.
49. Hudon, M., and E. J. LeRoux. 1986. Biology and population dynamics of the European corn borer (Ostrinia nubilalis) with special reference to sweet corn in Quebec. III. Population dynamics and spatial distribution. Phytoprotection. 67: 93-115.
50. James, D. G. 2003. Field evaluation of herbivore-induced plant volatiles as attractants for beneficial insects: methyl salicylate and the green lacewing, Chrysopa nigricornis. J. Chem. Ecol. 29: 1601-1609.
51. Jasinski, J. R., J. B. Eisley, C. E. Young, J. Kovach, and H. Willson. 2003. Select nontarget arthropod abundance in transgenic and nontransgenic field crops in Ohio. Environ. Entomol. 32: 407-413.
52. Jepson, P. C. 1989. Pesticides and nontarget invertebrates. Intercept Wimborne, Dorset, UK.
53. Kidd, N.A.C., and M. A. Jervis. 1996. Population dynamics, pp. 293-374. In M. A. Jervis and N.A.C. Kidd (eds.), Insect natural enemies. Chapman & Hall, New York, NY.
54. Kiman, Z. B., and K. V. Yeargan. 1985. Development and reproduction of the predator Orius insidiosus (Hemiptera: Anthocoridae) reared on diets of selected plant material and arthropod prey. Ann. Entomol. Soc. Am. 78: 464-467.
55. Koolhaas, J. E., C.A.M. Van Gestel, J. Römbke, A.M.V.M. Soares, and S. E. Jones. 2004. Ring-testing and field-validation of a terrestrial model ecosystem (TME) - an instrument for testing potentially harmful substances: effects of carbendazim on soil microarthropod communities. Ecotoxicology. 13: 75-88.
56. Lee, M. K., F. S. Walters, H. Hart, N. Palekar, and J.-S. Chen. 2003. The mode of action of the Bacillus thuringiensis vegetative insecticidal protein Vip3a differs from that of Crylab δ-endotoxin. Appl. Environ. Microbiol. 2003. 69: 4648-4657.
57. Leonard, A. W., R. V. Hyne, R. P. Lim, F. Pablo, and P. J. Van den Brink. 2000. Riverine endosulfan concentrations in the Namoi River, Australia: link to cotton field runoff and macroinvertebrate population densities. Environ. Toxicol. Chem. 19:1540-1551.
58. Lopez, M. D., J. R. Prasifka, D. J. Bruck, and L. C. Lewis. 2005. Utility of ground beetle species in field tests of potential non-target effects of Bt crops. Environ. Entomol. 34: 1317-1324.
59. Lozzia, G. C. 1999. Biodiversity and structure of ground beetle assemblages (Coleoptera, Carabidae) in Bt corn and its effect on non target insects. Boll. Zool. Agr. Bachic. 31: 37-58.
60. Lozzia, G., C. Furlanis, B. Manachini, and I. Rigamonti. 1999. Effects of Bt corn on Rhodopalosiphum padi (Rhynchota, Aphidiae) and its predator Chrysoperla carnea Stephen (Neuroptera, Chrysopidae). Boll. Zool. Agr. Bachic. 30: 153-164.
61. Luck, R. F., B. M. Shepard, and P. E. Kenmore. 1988. Experimental methods for evaluating arthropod natural enemies. Annu. Rev. Entomol. 33: 367-391.
62. Malone, L., and M. Pham-Delègue. 2001. Effects of transgene products on honey bees (Apis mellifera) and bumblebees (Bombus sp.). Apidologie. 32: 87-304.
63. McMurty, J. A., C. B. Huffaker, and M. van de Vrie. 1970. Ecology of tetranychid mites and their natural enemies: a review. I. Tetranychid enemies: their biological characters and impact of spray practices. Hilgardia. 40: 331-390.
64. Michels, G. J., and R. W. Behle. 1992. Evaluation of sampling methods for lady beetles (Coleoptera: Coccinellidae) in grain sorghum. J. Econ. Entomol. 85: 2251-2257.
65. Mihm, J. A., and H. C. Chiang. 1976. Laboratory studies of the life cycle and reproduction of some soil- and manure-inhabiting predatory mites (Acarina: Laelapidae). Pedobiologia. 16: 353-363.
66. Moar, W. J., M. Eubanks, B. Freeman, S. Turnipseed, J. Ruberson, and G. Head. 2002. Effects of Bt cotton on biological control agents in the southeastern United States, pp. 275-277. In R. G. Van Driesche (ed.), Proceedings of the First International Symposium on Biological Control of Arthropods. U.S. Dep. Agric. Forest Service, Morgantown, WV.
67. Moore, J. C., R. J. Snider, and L. S. Robertson. 1984. Effects of different management practices on Collembola and Acari in corn production systems. I. The effects of notillage and atrazine. Pedobiologia. 26: 143-152.
68. Naranjo, S. E. 2005. Long-term assessment of the effects of transgenic Bt cotton on the abundance of non-target arthropod natural enemies. Environ. Entomol. 34: 1193-1210.
69. Naranjo, S. E., and P. C. Ellsworth. 2002. Arthropod communities and transgenic cotton in the western United States: implications for biological control, pp. 284-291. In R. G. Van Driesche (ed.), Proceedings of the First International Symposium on Biological Control of Arthropods. U.S. Dep. Agric. Forest Service, Morgantown, WV.
70. National Agricultural Statistics Service [NASS]. 2004. Field corn acreage: biotechnology varieties. http://usda.-mannlib.cornell.edu/reports/ nassr/field/pcp-bba/acrg0604.txt.
71. Ockroy, M.L.B., T.C.J. Turlings, P. J. Edwards, M. E. Fritzsche-Hoballah, L. Ambrosetti, P. Bassetti, and S. Dorn. 2001. Response of natural populations of predators and parasitoids to artificially induced volatile emissions in maize plants (Zea mays L.). Agric. Forest Entomol. 3: 201-209.
72. Orr, D. B., and D. A. Landis. 1997. Oviposition of European corn borer (Lepidoptera: Pyralidae) and impact of natural enemy populations in transgenic versus isogenic corn. J. Econ. Entomol. 90: 905-909.
73. Ostlie, K. R., W. D. Hutchison, and R. L. Hellmich. 1997. Bt corn and European corn borer. University of Minnisota, St. Paul, MN.
74. Pakeman, R. J. 2004. Consistency of plant species and trait responses to grazing along a productivity gradient: a multi-site analysis. J. Ecol. 92: 893-905.
75. Pennan, D. R., and R. B. Chapman. 1988. Pesticide-induced mite ourbreaks: pyrethroids and spider mites. Exp. Appl. Acal. 4: 265-276.
76. 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.
77. Potting, R.P.J., L.E.M. Vet, and M. Dicke. 1996. Host microhabitat location by the stemborer parasitoid Cotesia flavipes: the role of locally and systemically induced plant volatiles. J. Chem. Ecol. 21: 525-539.
78. Prasifka, J. R., R. L. Hellmich, G. P. Dively, and L. C. Lewis. 2005. Assessing the effects of pest management on non-target arthropods: the influence of plot size and isolation. Environ. Entomol. 34: 1181-1192.
79. Rafalimanana, H., L. Kaiser, and J. M. Delpuech. 2002. Stimulating effects of the insecticide chlorpyrifos on host searching and infestation efficacy of a parasitoid wasp. Pest Manag. Sci. 58: 321-328.
80. Reddy, G.V.P. 2002. Plant volatiles mediate orientation and plant preference by the predator Chrysoperla carnea Stephens (Neuroptera: Chrysopidae). Biol. Control. 25: 49-55.
81. Reed, G. L., A. S. Jensen, J. Riebe, G. Head, and J. J. Duan. 2001. Transgenic Bt potato and conventional insecticides for Colorado potato beetle management: comparative efficacy and non-target impacts. Entomol. Exp. Appl. 100: 89-100.
82. 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.
83. Riddick, E. W., G. Dively, and P. Barbosa. 1998. Effect of a seed-mix deployment of Cry3A-transgenic and non-transgenic potato on the abundance of Lebia grandis (Coleoptera: Carabidae) and Coleomegilla maculata (Coleoptera: Coccinellidae). Ann. Entomol. Soc. Am. 91: 647-653.
84. Romeis, J., A. Dutton, and F. Bigler. 2004. Bacillus thuringiensis toxin (Cry1Ab) has no direct effect on larvae of the green lacewing, Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae). J. Insect Physiol. 50: 175-183.
85. Russek-Cohen, E., and L. W. Douglas. 1999. Mixed models data analysis: using PROC MIXED for biological research. Mixed model shortcourse manual. University of Maryland, College Park, MD.
86. SAS Institute. 1997. SAS user's guide. SAS Institute, Cary, NC.
87. Saxena, D., and G. Stotzky. 2001. Bacillus thuringiensis (Bt) toxin released from root exudates and biomass of Bt corn has no apparent effect on earthworms, nematodes, protozoa, bacteria, and fungi in soil. Soil Biol. Biochem. 33: 1225-1230.
88. Saxena, D., S. Flores, and G. Stotzky. 1999. Insecticidal toxin in root exudates from Bacillus thuringiensis corn. Nature (Lond.). 402: 480.
89. Schuler, T. H. 2003. Tritrophic choice experiments with Bt plants, the diamondback moth (Plutella xylostella) and the parasitoid Cotesia plutellae. Transgenic Res. 12: 351-361.
90. Schuler, T. H., G. M. Poppy, B. R. Kerry, and I. Denholm. 1999a. Potential side effects of insect-resistant transgenic plants on arthropod natural enemies. Trends Biotechnol. 17: 210-216.
91. Schuler, T. H., R.P.J. Potting, I. Denholm, and G. M. Poppy. 1999b. Parasitoid behaviour and Bt plants. Nature (Lond.). 400: 825.
92. Shannon, C. E., and W. Weaver. 1949. The mathematical theory of communication. University of Illinois Press, Urbana, IL.
93. Sims, S. R. 1995. Bacillus thuringiensis var. kurstaki [CryIA (C)] protein expressed in transgenic cotton: effects on beneficial and other non-target insects. Southwest. Entomol. 20: 493-500.
94. Sims, S. R., and J. W. Martin. 1997. Effect of the Bacillus thuringiensis insecticidal proteins CryIA(b), CryIA(c), CryIIA, and CryIIIA of Folsomia candida and Xenylla grisea (Insecta: Collembola). Pedobiologia. 41: 412-416.
95. Sisterson, M. S., R. W. Biggs, C. Olson, Y. Carriere, T. J. Dennehy, and B. E. Tabashnik. 2004. Arthropod abundance and diversity in Bt and non-Bt cotton fields. Environ. Entomol. 33: 921-929.
96. Smit, C. E., A. J. Schouten, P. J. Van den Brink, M.L.P. van Esbroek, and L. Posthuma. 2002. Effects of zinc contamination on a natural nematode community in outdoor soil mesocosms. Arch. Environ. Contam. Toxicol. 42: 205-216.
97. Steffey, K. L., M. E. Rice, J. All, D. A. Andow, M. E. Gray, and J. W. Van Duyn. 1999. Handbook of corn insects. Entomology Society of America, Lanham, MD.
98. Steffey, K. L., M. Venditti, B. Ria Barrido, and A. S. Felsot. 2004. Effect of Bacillus thuringiensis corn on natural enemies of the European corn borer. Agricultural biotechnology: challenges and prospects. American Chemical Society, Washington, DC.
99. Strong, D. 1997. Subterranean insect-plant foodwebs: strange natural enemies and their enemies. Bull. Ecol. Soc. Am. 78(Suppl 4):192.
100. Tapp, H., and G. Stotzky. 1998. Persistence of the insecticidal toxin from Bacillus thuringiensis subsp. kurstaki in soil. Soil Biochem. 30: 471-476.
101. Theiling, K. M., and B. A. Croft. 1988. Pesticide side-effects on arthropod natural enemies - a database summary. Agric. Ecosystems Environ. 21: 191-218.
102. Torres, J. B. and J. R. Ruberson. 2005. Canopy-and ground-dwelling predatory arthropods in Bt and non-Bt cotton fields: patterns and mechanisms. Environ. Entomol. 34: 1242-1256.
103. Turlings, T.C.J., J. H. Tumlinson, and W. J. Lewis. 1990. Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science. 250: 1251-3.
104. Turlings, T.C.J., H. T. Alborn, J. H. Loughrin, and J. H. Tumlinson. 2000. Volicitin, an elicitor of maize volatiles in oral secretion of Spodoptera exigua: isolation and bioactivity. J. Chem. Ecol. 26: 189-202.
105. Turlings, T.C.J., M. Bernasconi, R. Bertossa, F. Bigler, G. Caloz, and S. Dorn. 1998. The introduction of volatile emissions in maize by three herbivore species with different feeding habits: possible consequences for their natural enemies. Biol. Control. 11: 122-129.
106. Tyler, B.M.J., and C. R. Ellis. 1979. Ground beetles in three tillage plots in Ontario and observations on their importance as predators of the northern corn rootworm, Diabrotica longicornis (Coleoptera: Chrysomelidae). Proc. Entomol. Soc. Ontario. 110: 65-73.
107. Udayagiri, S., C. E. Mason, and J. D. Pesek Jr. 1997. Coleomegilla maculata, Coccinella septempunctata (Coleoptera: Coccinellidae), Chrysoperla carnea (Neuroptera: Chrysopidae), and Macrocentrus grandii (Hymenoptera: Braconidae) trapped on colored sticky traps in corn habitats. Environ. Entomol. 26: 983-988.
108. Wheeler, A.G.J., and C. A. Stoops. 1996. Status and spread of the Palearctic lady beetles Hippodamia variegata and Propylea quatuordecimpunctata (Coleoptera: Coccinellidae) in Pennsylvania, 1993-1995. Entomol. News. 107: 291-298.
109. Whitehouse, M.E.A., L. J. Wilson, and G. P. Fitt. 2005. A comparison of arthropod communities in transgenic Bt and conventional cotton in Australia. Environ. Entomol. 34: 1224-1241.
110. Whitman, D. 1988. Allelochemical interactions among plants, herbivores and their predators, pp. 11-64. In P. Barbosa and D. Letourneau (eds.), Novel aspects of insect-plant interactions. Wiley, New York.
111. Wilson, L. J., L. R. Bauer, and D. A Lally. 1999. Insecticide-induced increases in aphid abundance in cotton. Aust. J. Entomol. 3: 242-243.
112. Van Emden, H. F., and K. S. Hagen. 1976. Olfactory reactions of the green lacewing, Chrysopa camea, to tryptophan and certain breakdown products. Environ. Entomol. 5: 469-473.
113. Venditti, M. E., and K. L. Steffey. 2003. Field effects of Bt corn on the impact of parasitoids and pathogens on european corn borer in Illinois, pp. 278-283. In R. G. Van Driesche (ed.), Proceedings of the First International Symposium on Biological Control of Arthropods. U.S. Dep. Agric. Forest Service, Morgantown, WV.
114. Vet, L.E.M., and M. Dicke. 1992. Ecology of infochemical use by natural enemies in a tritrophic context. Annu. Rev. Entomol. 37: 141-172.
115. Yu, C.-G., M. A. Mullins, G. W. Warren, M. G. Koziel, and J. J. Estruch. 1997. The Bacillus thuringiensis vegetative insecticidal protein Vip3A lyses midgut epithelium cells of susceptible insects. Appl. Environ. Microbiol. 63: 532-536.
116. Yu, L., R. E. Berry, and B. A. Croft. 1997. Effects of Bacillus thuringiensis toxins in transgenic cotton and potato on Folsomia candida (Collembola: Isotomidae) and Oppia nitens (Acari: Orbatidae). J. Econ. Entomol. 90: 113-118.
117. Zhu, J., A. A. Cosse, J. J. Obrycki, K. S. Boo, and T. C. Baker. 1999. Olfactory reactions of the twelve-spotted lady beetle, Coleomegilla maculata and the green lacewing, Chrysoperla carnea to semiochemicals released from their prey and host plant: electroantennogram and behavioral responses. J. Chem. Ecol. 25: 1163-1177.
118. 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: 846-50.