The impact of Cry3Bb Bt-maize on two guilds of beneficial beetles

Agriculture, Ecosystems and Environment

Volumn 156, Issue , 2012, Pages 72-81

  Stephens, Erin J ^a   Losey, John E ^a   Allee, Leslie L ^a   DiTommaso, Antonio ^a   Bodner, Carrie ^a   Breyre, Amelia ^a  

^a Cornell University ^*  (United States)

Author keywords

Bt; Carabids; Coccinellids; Cry3; Non target impacts; Transgenic maize

Indexed keywords

APHID; BEETLE; CHEMICAL CONTROL; INSECTICIDE; MAIZE; NONTARGET ORGANISM; PITFALL TRAP; PROTEIN; TRANSGENIC PLANT; TRITROPHIC INTERACTION;

AGONUM MUELLERI; APHIDIDAE; CARABIDAE; COCCINELLIDAE; COLEOPTERA; HARMONIA AXYRIDIS; POECILUS LUCUBLANDUS; ZEA MAYS;

EID: 84861435480     PISSN: 01678809     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.agee.2012.05.002     Document Type: Article

References (61)

1. Agdia Incorporated Agdia Product Documentation PathoScreen kit for Bt-Cry3Bb1 ELISA 2004, Agdia Incorporated, Elkhard, IN, USA. http://www.agdia.com/cgi_bin/catalog.cgi?m130.2.1.
2. Auclair J.L. Host plant resistance. World Crop Pests: Aphids Their Biology, Natural Enemies and Control 1989, 1-311. Elsevier, New York. A.K. Minks, P. Harrewijn (Eds.).
3. Bai Y.Y., Jiang M.X., Cheng J.A. Effects of transgenic cry1Ab rice pollen on fi{ligature}tness of Propylea japonica (Thunberg). J. Pest. Sci. 2005, 78:123-128.
4. Best R.L., Beegle C.C. Food preferences of five species of carabids commonly found in Iowa cornfields. Environ. Entomol. 1977, 6:9-12.
5. Brust G.E., Stinner B.R., McCartney D. Tillage and soil insecticide effects on predator-black cutworm interactions in corn agroecosystems. J. Econ. Entomol. 1985, 78:1389-1392.
6. Brust G.E., Stinner B.R., McCartney D. Predator activity and predation in corn agroecosystems. Environ. Entomol. 1986, 15:1017-1021.
7. Cardina J., Norquay H.M., Stinner B.R., McCarthy D.A. Postdispersal predation of velvetleaf (Abutilon theophrasti) seeds. Weed Sci. 1996, 44:534-539.
8. Changming W.F.C. Studies on the structure of the rice pest-natural enemy community and diversity under IPM area and chemical control area. Acta Ecolog. Sin. 1986, cnki:ISSN:1000-0933.0.1986-02-009.
9. Chen Z.Z., Willson H.R. The impact of insecticides on ground beetles in corn. Poster. 1996 Ent. Soc. Amer. Annual Meeting 1996, http://www.entomology.wisc.edu/mbcn/field405.html.
10. Devare M., Londono-R L.M., Thies J.E. Neither transgenic Bt maize (MON863) nor tefluthrin insecticide adversely affect soil microbial activity or biomass: a 3-year field analysis. Soil Biol. Biogeochem. 2007, 39:2038-2047.
11. Demoute J.P. A brief review of the environmental fate and metabolism of pyrethroids. Pestic. Sci. 1989, 27:375-385.
12. Down R.E., Ford L., Woodhouse S.D., Davison G.M., Majerus M.E.N., Gatehouse J.A., Gatehouse A.M.R. 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. 2003, 12:229-241.
13. Dritschilo W., Wanner D. Ground beetle abundance in organic and conventional corn fields. Environ. Entomol. 1980, 9:629-631.
14. Evans E.W. Numerical responses of aphid predators to varying prey density among Utah alfalfa fields. J. Kans. Entomol. Soc. 1992, 65:30-38.
15. Ferry N., Mulligan E.A., Stewart C.N., Tabashnik B.E., Port G.R., Gatehous A.M.R. Prey-mediated effects of transgenic canola on a benefi{ligature}cial, non-target, carabid beetle. Transgen. Res. 2006, 15:501-514.
16. Floate K.D., Cárcamo H.A., Blackshaw R.E., Postman B., Bourassa S. Response of ground beetle (Coleoptera: Carabidae) field populations to four years of Lepidoptera-specific Bt corn production. Environ. Entomol. 2007, 36:1269-1274.
17. Garcia M., Ortego F., Castanera P., Farinos G.P. Effects of exposure to the toxin Cry1Ab through Bt maize fed-prey on the performance and digestive physiology of the predatory rove beetle Atheta coriaria. Biol. Control 2010, 55:225-233.
18. González-Zamora J.E., Camúñez S., Avilla C. Effects of Bacillus thuringiensis Cry toxins on developmental and reproductive characteristics of the predator Orius albidipennis (Hemiptera: Anthocoridae) under laboratory conditions. Environ. Entomol. 2007, 36:1246-1253.
19. Gray M.E. Prescriptive use of transgenic hybrids for corn rootworms: an ominous cloud on the horizon?. Crop Protection Technology Conference 2000, 97-103.
20. Gould F., Kennedy G.G., Johnson M.T. Effects of natural enemies on the rate of herbivore adaptation to resistant host plants. Entomol. Exp. Appl. 1991, 58:1-14.
21. Harwood J.D., Wallin W.G., Obrycki J.J. Uptake of Bt endotoxins by nontarget herbivores and higher order arthropod predators: molecular evidence from a transgenic corn agroecosystem. Mol. Ecol. 2005, 14:2815-2823.
22. Hodek I., Honek A. The Ecology of Coccinellidae 1996, Kluwer Academic Publishers, Boston, MA.
23. Hoheisel G.A., Fleischer S.J. Coccinellids, aphids, and pollen in diversified vegetable fields with transgenic and isoline cultivars. J. Insect Sci. 2007, 7:61.
24. Iperti G. Biodiversity of predaceous coccinellidae in relation to bioindication and economic importance. Agric. Ecosyst. Environ. 1999, 74:323-342.
25. Jost L. Entropy and diversity. Oikos 2006, 113:363-375.
26. Koch R.L. The multicolored Asian lady beetle, Harmonia axyridis: a review of its biology, uses in biological control, and non-target impacts. J. Insect Sci. 2003, 3:1-16.
27. Lesiewicz D.S., Van-duyn J.W., Bradley J.R. Mid season response of 3 carabids to soil insecticides applied to field corn plots at planting. J. Ga. Entomol. Soc. 1984, 19:271-275.
28. Leslie T.W., Biddinger D.J., Mullin C.A., Fleischer S.J. Carabidae population dynamics and temporal partitioning: response to coupled neonicotinoid-transgenic technologies in maize. Environ. Entomol. 2009, 38:935-943.
29. Leslie T.W., Biddinger D.J., Rohr J.R., Fleischer S.J. Conventional and seed-based insect management strategies similarly influence nontarget Coleopteran communities in maize. Environ. Entomol. 2010, 39:2045-2055.
30. Li Y., Romeis J. Bt maize expressing Cry3Bb1 does not harm the spider mite, Tetranychus urticae, or its ladybird beetle predator, Stethorus punctillum. Biol. Control 2010, 53:337-344.
31. Losey J.E., Vaughan M. The economic value of ecological services provided by insects. Bioscience 2006, 56:311-323.
32. Losey J.E., Rayor L.S., Carter M.E. Transgenic pollen harms monarch larvae. Nature 1999, 399:214.
33. Lövei G.L., Andow D.A., Arpaia S. Transgenic insecticidal crops and natural enemies: a detailed review of laboratory studies. Environ. Entomol. 2009, 38:293-306.
34. Lumbierres B., Albajes R., Pons X. Transgenic Bt maize and Rhopalosiphum padi (Hom., Aphididae) performance. Ecol. Entomol. 2004, 29:309-317.
35. Lund R.D., Turpin F.T. Carabid damage to weed seeds found in Indiana cornfields. Environ. Entomol. 1977, 6:695-698.
36. Marino P.C., Gross K.L., Landis D.A. Weed seed loss due to predation in Michigan maize fields. Agric. Ecosyst. Environ. 1997, 66:189-196.
37. Meissle M., Vojtech E., Poppy G.M. Effects of Bt maize-fed prey on the generalist predator Poecilus cupreus L. (Coleoptera: Carabidae). Transgen. Res. 2005, 14:123-132.
38. Metcalf R.L. Foreward. Methods for the Study of Pest Diabrotica 1986, 1-12. Springer-Verlag, New York. J.L. Krysan, T.A. Miller (Eds.).
39. Moser S.E., Harwood J.D., Obryck J.J. Larval feeding on Bt hybrid and Non-Bt corn seedlings by Harmonia axyridis (Coleoptera: Coccinellidae) and Coleomegilla maculata (Coleoptera: Coccinellidae). Environ. Entomol. 2008, 37:525-533.
40. Naranjo S.E. Long-term assessment of the effects of transgenic Bt cotton on the abundance of nontarget arthropod natural enemies. Environ. Entomol. 2005, 34:1193-1210.
41. Obrist L.B., Dutton A., Albajes R., Bigler F. Exposure of arthropod predators to Cry1Ab toxin in Bt maize fields. Ecol. Entomol. 2006, 31:143-154.
42. Obrycki J.J., Losey J., Taylor O., Jesse L.C.H. Transgenic insecticidal corn: beyond insecticidal toxicity to ecological complexity. Bioscience 2001, 51:353-361.
43. Ott L. An Introduction to Statistical Methods and Data Analysis 1988, PWS-Kent, Boston, MA. 3rd ed.
44. Peterson J.A., Obrycki J.J., Harwood J.D. Quantification of Bt-endotoxin exposure pathways in carabid food webs across multiple transgenic events. Biocontrol Sci. Technol. 2009, 19:613-625.
45. Rauschen S., Schaarschmidt F., Gathmann A. Occurrence and fi{ligature}eld densities of Coleoptera in the maize herb layer: implications for environmental risk assessment of genetically modifi{ligature}ed Bt-maize. Transgen. Res. 2010, 19:727-744.
46. Reed J.P., Hall F.R., Krueger H.R. Contact and volatile toxicity of insecticides to black cutworm larvae (Lepidoptera: Noctuidae) and carabid beetles (Coleoptera: Carabidae) in soil. J. Econ. Entomol. 1992, 85:256-261.
47. SAS Institute SAS/STAT User's Guide: Version 6 1990, vol. 2. SAS Institute, Cary, NC, USA. 4th ed.
48. Saxena D., Flores S., Stotzky G. Transgenic plants: insecticidal toxin in root exudates from Bt corn. Nature 1999, 402:480.
49. Saxena D., Stotzky G. Bt corn has a higher lignin content than non-Bt corn. Am. J. Bot. 2001, 88:1704-1709.
50. Schmidt J.E.U., Braun C.U., Whitehouse L.P., Hilbeck A. Effects of activated Bt transgene products (Cry1Ab, Cry3Bb) on immature stages of the ladybird Adalia bipunctata in laboratory ecotoxicity testing. Arch. Environ. Contam. Toxicol. 2009, 56:221-228.
51. Shields E.J., Sher R.B., Taylor P.S. Sequential sampling plan for Northern and Western corn rootworm. J. Econ. Entomol. 1991, 84:165-169.
52. Shuler R.E., DiTommaso A., Losey J.E., Mohler C.L. Postdispersal weed seed predation is affected by experimental substrate. Weed Sci. 2008, 56:889-895.
53. Snyder W.E., Synder G.B., Finke D.L., Straub C.S. Predator biodiversity strengthens herbivore suppression. Ecol. Lett. 2006, 9:789-796.
54. Steffey K., Rice M., All J., Andow D., Gray M., Van Duyn J.W. Handbook of Corn Insects 1999, Entomological Society of America, Lanham, MD, USA.
55. Tarkalson D.D., Kachman S.D., Knopps J.M.N., Thies J.E., Wortman C.S. Decomposition of Bt and non-Bt corn hybrid residues in the field. 2008. Nutr. Cycl. Agroecosyst. 2008, 80:211-222.
56. Torres J.B., Ruberson J.R. Canopy- and ground-dwelling predatory arthropods in commercial Bt and non-Bt cotton fields: patterns and mechanisms. Environ. Entomol. 2005, 34:1242-1256.
57. Toschki A., Hothorn L.A., Roß-Nickoll M. Effects of cultivation of genetically modified Bt maize on epigeic arthropods (Araneae: Carabidae). Environ. Entomol. 2007, 36:967-981.
58. Wolfenbarger L.L., Naranjo S.E., Lundgren J.G., Bitzer R.J., Watrud L.S. Bt crop effects on functional guilds of non-target arthropods: a meta-analysis. PLoS One 2008, 3(5):e2118.
59. Yasuda H., Evans E.W., Kajita Y., Urakawa K., Takizawa T. Asymmetrical larval interactions between introduced and indigenous ladybirds in North America. Oecologia 2004, 141:722-731.
60. Zurbrugg C., Nentwig W. Ingestion and excretion of two transgenic Bt corn varieties by slugs. Transgen. Res. 2009, 18:215-225.
61. Zwahlen C., Andow D.A. Field evidence for the exposure of ground beetles to Cry1Ab from transgenic corn. Environ. Biosafety Res. 2005, 4:113-117.