Laboratory toxicity studies demonstrate no adverse effects of Cry1Ab and Cry3Bb1 to larvae of Adalia bipunctata (Coleoptera: Coccinellidae): The importance of study design

Transgenic Research

Volumn 20, Issue 3, 2011, Pages 467-479

  Álvarez Alfageme, Fernando ^a   Bigler, Franz ^a   Romeis, Jörg ^a  

^a AGROSCOPE RECKENHOLZ TÄNIKON RESEARCH STATION ART   (Switzerland)

Author keywords

Environmental risk assessment; MON810; MON88017; Non target effects; Study design

Indexed keywords

BACTERIAL PROTEIN; CRY3BBL ENDOTOXIN, BACILLUS THURINGIENSIS; ENDOTOXIN; HEMOLYSIN; INSECTICIDAL CRYSTAL PROTEIN, BACILLUS THURINGIENSIS;

ANIMAL; ARTICLE; BACILLUS THURINGIENSIS; BEETLE; GENETICS; LARVA; MAIZE; METABOLISM; METHODOLOGY; PHYSIOLOGY; RISK ASSESSMENT; TETRANYCHIDAE; TRANSGENIC PLANT;

ANIMALS; BACILLUS THURINGIENSIS; BACTERIAL PROTEINS; BEETLES; ENDOTOXINS; HEMOLYSIN PROTEINS; LARVA; PLANTS, GENETICALLY MODIFIED; RESEARCH DESIGN; RISK ASSESSMENT; TETRANYCHIDAE; ZEA MAYS;

ACARI; ADALIA BIPUNCTATA; ARANEAE; COCCINELLIDAE; COLEOPTERA; TETRANYCHIDAE; ZEA MAYS;

EID: 79955858162     PISSN: 09628819     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11248-010-9430-5     Document Type: Article

References (67)

1. Ahmad A, Wilde GE, Whitworth RJ, Zolnerowich G (2006) Effect of corn hybrids expressing the coleopteran-specific Cry3Bb1 protein for corn rootworm control on aboveground insect predators. J Econ Entomol 99: 1085-1095.
2. Álvarez-Alfageme F, Ferry N, Castañera P, Ortego F, Gatehouse AMR (2008) Prey mediated effects of Bt maize on fitness and digestive physiology of the red spider mite predator Stethorus punctillum Weise (Coleoptera: Coccinellidae). Transgenic Res 17: 943-954.
3. Banks CJ (1957) The behaviour of individual coccinellid larvae on plants. Br J Anim Behav 5: 12-24.
4. Bhatti MA, Duan J, Head GP, Jiang C, McKee MJ, Nickson TE, Pilcher CL, Pilcher CD (2005) Field evaluation of the impact of corn rootworm (Coleoptera: Chrysomelidae)-protected Bt corn on foliage-dwelling arthropods. Environ Entomol 34: 1336-1345.
5. Blackman RL (1967) The effects of different aphid foods on Adalia bipunctata L. and Coccinella 7-punctata L. Ann appl Biol 59: 207-219.
6. BVL (2009) Bekanntmachung eines Bescheides zur Beschränkung des Inverkehrbringens von gentechnischen veränderten Mais der Linie MON810. Federal Office of Consumer Protection and Food Safety (BVL), Berlin, Germany. http://www. bvl. bund. de/cln_027/DE/08__PresseInfothek/00__doks__downloads/mon__810__bescheid, templateId=raw, property=publicationFile. pdf/mon_810_bescheid. pdf. Accessed 6 July 2010.
7. CERA (2010) GM Crop Database. Center for Environmental Risk Assessment (CERA), Washington, DC. http://cera-gmc. org/index. php?action=gm_crop_database. Accessed 6 July 2010.
8. Daly T, Buntin GD (2005) Effects of Bacillus thuringiensis transgenic corn for lepidopteran control on non-target arthropods. Environ Entomol 34: 1292-1301.
9. De Clercq P, Bonte M, van Speybroeck K, Bolckmans K, Deforce K (2005) Development and reproduction of Adalia bipunctata (Coleoptera: Coccinellidae) on eggs of Ephestia kuehniella (Lepidoptera: Phycitidae) and pollen. Pest Manag Sci 61: 1129-1132.
10. De la Poza M, Pons X, Farinós GP, López C, Ortego F, Eizaguirre M, Castañera P, Albajes R (2005) Impact of farm-scale Bt maize on abundance of predatory arthropods in Spain. Crop Prot 24: 677-684.
11. Dhillon MK, Sharma HC (2009) Effects of Bacillus thuringiensis δ-endotoxins Cry1Ab and Cry1Ac on the coccinellid beetle, Cheilomenes sexmaculatus (Coleoptera, Coccinellidae) under direct and indirect exposure conditions. Biocontr Sci Technol 19: 407-420.
12. Dixon AFG (1959) An experimental study of the searching behaviour of the predatory coccinellid beetle Adalia decempunctata (L.). J Anim Ecol 28: 259-281.
13. Duan JJ, Head G, McKee MJ, Nickson TE, Martin JW, Sayegh FS (2002) Evaluation of dietary effects of transgenic corn pollen expressing Cry3Bb1 protein on a non-target ladybird beetle, Coleomegilla maculata. Ent Exp Appl 104: 271-280.
14. Duan JJ, Paradise MS, Lundgren JG, Bookout JT, Jian C, Wiedenmann RN (2006) Assessing non-target impacts of Bt corn resistant to corn rootworms: Tier-1 testing with larvae of Poecilus chalcites (Coleoptera: Carabidae). Environ Entomol 35: 135-142.
15. Duan JJ, Teixeira D, Huesing JE, Jiang C (2008) Assessing the risk to nontarget organisms from Bt corn resistant to corn rootworms (Coleoptera: Chrysomelidae): Tier-I testing with Orius insidiosus (Heteroptera: Anthocoridae). Environ Entomol 37: 838-844.
16. Duan JJ, Lundgren JG, Naranjo S, Marvier M (2010) Extrapolating non-target risk of Bt crops from laboratory to field. Biol Lett 6: 74-77.
17. Dutton A, Klein H, Romeis J, Bigler F (2002) Uptake of Bt-toxin by herbivores feeding on transgenic maize and consequences for the predator Chrysoperla carnea. Ecol Entomol 27: 441-447.
18. EFSA (2009) Statistical considerations for the safety evaluation of GMOs. European Food Safety Authority (EFSA), Parma. http://www. efsa. europa. eu/EFSA/efsa_locale-1178620753812_1211902768517. htm. Accessed 6 July 2010.
19. Garcia-Alonso M, Jacobs E, Raybould A, Nickson TE, Sowig P, Willekens H, van der Kouwe P, Layton R, Amijee F, Fuentes AM, Tencalla F (2006) A tiered system for assessing the risk of genetically modified plants to non-target organisms. Environ Biosafety Res 5: 57-65.
20. Glare TR, O'Callaghan M (2000) Bacillus thuringiensis: biology, ecology and safety. Wiley, Chichester.
21. Hagen KS (1962) Biology and ecology of predaceous Coccinellidae. Annu Rev Entomol 7: 289-326.
22. Harwood JD, Wallin WG, Obrycki JJ (2005) Uptake of Bt endotoxins by nontarget herbivores and higher order arthropod predators: molecular evidence from a transgenic corn agroecosystem. Mol Ecol 14: 2815-2823.
23. Harwood JD, Samson RA, Obrycki JJ (2007) Temporal detection of Cry1Ab-endotoxins in coccinellid predators from fields of Bacillus thuringiensis corn. Bull Ent Res 97: 643-648.
24. Head G, Brown CR, Groth ME, Duan JJ (2001) Cry1Ab protein levels in phytophagous insects feeding on transgenic corn: implications for secondary exposure risk assessment. Ent Exp Appl 99: 37-45.
25. Hellmich RL, Albajes R, Bergvinson D, Prasifka JR, Wang ZY, Weiss MJ (2008) The present and future role of insect-resistant genetically modified maize in IPM. In: Romeis J, Shelton AM, Kennedy GG (eds) Integration of insect-resistant genetically modified crops within IPM programs. Springer, New York, pp 119-158.
26. Hodek I, Honěk A (1996) Ecology of Coccinellidae. Kluwer, Dordrecht.
27. Hogervorst PAM, Ferry N, Gatehouse AMR, Wäckers FL, Romeis J (2006) Direct effects of snowdrop lectin (GNA) on larvae of three aphid predators and fate of GNA after ingestion. J Insect Phys 52: 614-624.
28. Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6: 65-70.
29. Hurst GDD, Majerus MEN (1993) Why do maternally inherited microorganisms kill males? Heredity 71: 81-95.
30. ICH (2005) Harmonised tripartite guideline: validation of analytical procedures: Text and methodology Q2(R1). In: International conference on harmonisation of technical requirements for registration of pharmaceuticals for human use. http://www. ich. org/LOB/media/MEDIA417. pdf. Accessed 6 July 2010.
31. James C (2009) Global status of commercialized biotech/GM crops: 2009. ISAAA Brief No. 41. ISAAA, Ithaca, NY.
32. Lawo NC, Romeis J (2008) Assessing the utilization of a carbohydrate food source and the impact of insecticidal proteins on larvae of the green lacewing, Chrysoperla carnea. Biol Contr 44: 389-398.
33. Li Y, Romeis J (2010) Bt maize expressing Cry3Bb1 does not harm the spider mite, Tetranychus urticae, or its ladybird beetle predator, Stethorus punctillum. Biol Contr 53: 337-344.
34. Lundgren JG, Wiedenmann RN (2002) Coleopteran-specific Cry3Bb toxin from transgenic corn pollen does not affect the fitness of a nontarget species, Coleomegilla maculata DeGeer (Coleoptera: Coccinellidae). Environ Entomol 31: 1213-1218.
35. Lundgren JG, Wiedenmann RN (2005) Tritrophic interactions among Bt (Cry3Bb1) corn, aphid prey, and the predator Coleomegilla maculata (Coleoptera: Coccinellidae). Environ Entomol 34: 1621-1625.
36. Lundgren JG, Huber A, Wiedenmann RN (2005) Quantification of consumption of corn pollen by the predator Coleomegilla maculata (Coleoptera: Coccinellidae) during anthesis in an Illinois cornfield. Agric For Entomol 7: 53-60.
37. Meissle M, Romeis J (2008) Compatibility of biological control with Bt maize expressing Cry3Bb1 in controlling corn rootworms. In: Mason PG, Gillespie DR, Vincent C (eds). Proceedings of the third international symposium on biological control of arthropods, Christchurch, New Zealand, 8-13 February 2009, FHTET-2008-06, Morgantown, WV, United States Department of Agriculture, Forest Service, pp 145-160. http://www. biocontrol. ucr. edu/ISBCA/3. Accessed 6 July 2010.
38. Meissle M, Romeis J (2009a) Insecticidal activity of Cry3Bb1 expressed in Bt maize on larvae of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Ent Exp Appl 131: 308-319.
39. Meissle M, Romeis J (2009b) The web-building spider Theridion impressum (Araneae: Theridiidae) is not adversely affected by Bt maize resistant to corn rootworms. Plant Biotech J 7: 645-656.
40. ® Insect-Protected Corn Event MON 810. http://www. agbios. com/docroot/decdocs/02-269-010. pdf. Accessed 6 July 2010.
41. Monsanto (2004) Petition for the determination of nonregulated status for MON88017 corn. http://www. aphis. usda. gov/brs/aphisdocs/04_12501p. pdf. Accessed 6 July 2010.
42. Musser FR, Shelton AM (2003) Bt sweet corn and selective insecticides: Impacts on pests and predators. J Econ Entomol 96: 71-80.
43. Naranjo SE (2009) Impacts of Bt crops on non-target invertebrates and insecticide use patterns. CAB reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 4, No. 011. doi: 10. 1079/PAVSNNR20094011.
44. Nguyen HT, Jehle JJ (2007) Quantitative analysis of the seasonal and tissue-specific expression of Cry1Ab in transgenic maize Mon810. J Plant Dis Prot 114: 82-87.
45. Nguyen HT, Jehle JJ (2009) Expression of Cry3Bb1 in transgenic corn MON88017. J Agric Food Chem 57: 9990-9996.
46. Obrist L, Dutton A, Romeis J, Bigler F (2006a) Biological activity of Cry1Ab toxin expressed by Bt maize following ingestion by herbivorous arthropods and exposure of the predator Chrysoperla carnea. Biocontrol 51: 31-48.
47. Obrist LB, Dutton A, Albajes R, Bigler F (2006b) Exposure of arthropod predators to Cry1Ab toxin in Bt maize fields. Ecol Entomol 31: 143-154.
48. OGTR (2009) Risk analysis framework. Office of the Gene Technology Regulator, Canberra, Australia. http://www. health. gov. au/internet/ogtr/publishing. nsf/Content/riskassessments-1. Accessed 6 July 2010.
49. Pilcher CD, Obrycki JJ, Rice ME, Lewis LC (1997) Preimaginal development, survival, and field abundance of insect predators on transgenic Bacillus thuringiensis corn. Environ Entomol 26: 446-454.
50. Pilcher CD, Rice ME, Obrycki JJ (2005) Impact of transgenic Bacillus thuringiensis corn and crop phenology on five non-target arthropods. Environ Entomol 34: 1302-1316.
51. Porcar M, García-Robles I, Domínguez-Escribà L, Latorre A (2010) Effects of Bacillus thuringiensis Cry1Ab and Cry3Aa endotoxins on predatory Coleoptera tested through artificial diet-incorporation bioassay. Bull Ent Res 100: 297-302.
52. Raps A, Kehr J, Gugerli P, Moar WJ, Bigler F, Hilbeck A (2001) Immunological analysis of phloem sap of Bacillus thuringiensis corn and of the non-target herbivore Rhopalosiphum padi (Homoptera: Aphididae) for the presence of Cry1Ab. Mol Ecol 10: 525-533.
53. Rauschen S (2010) A case of "pseudo science"? A study claiming effects of the Cry1Ab protein on larvae of the two-spotted ladybird is reminiscent of the case of the green lacewing. Transgenic Res 19: 13-16.
54. Rauschen S, Schaarschmidt F, Gathmann A (2010) Occurrence and field densities of Coleoptera in the maize for environmental risk assessment of genetically modified Bt-maize. Transgenic Res 19. doi: 10. 1007/s11248-009-9351-3.
55. Ricroch A, Bergé JB, Kuntz M (2010) Is the German suspension of MON810 maize cultivation scientifically justified? Transgenic Res 19: 1-12.
56. Robinson AG (1951) Annotated list of predators of tetranchid mites in Manitoba. Annu Rep Entomol Soc Ont 82: 33-37.
57. Romeis J, Meissle M (2010) Non-target risk assessment of Bt crops-cry protein uptake by aphids. J Appl Ent 134. doi: 10. 1111/j. 1439-0418. 2010. 01546. x.
58. Romeis J, Meissle M, Bigler F (2006) Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nat Biotechnol 24: 63-71.
59. Romeis J, Bartsch D, Bigler F, Candolfi MP, Gielkens MMC, Hartley SE, Hellmich RL, Huesing JE, Jepson PC, Layton R, Quemada H, Raybould A, Rose RI, Schiemann J, Sears MK, Shelton AM, Sweet J, Vaituzis Z, Wolt JD (2008) Assessment of risk of insect-resistant transgenic crops to nontarget arthropods. Nat Biotechnol 26: 203-208.
60. Rose RI (ed) (2007) White paper on tier-based testing for the effects of proteinaceous insecticidal plant-incorporated protectants on non-target invertebrates for regulatory risk assessment. US Environmental Protection Agency, Washington, DC. http://www. epa. gov/pesticides/biopesticides/pips/non-target-arthropods. pdf. Accessed 6 July 2010.
61. Rose R, Dively GP (2007) Effects of insecticide-treated and lepidopteran-active Bt transgenic sweet corn on the abundance and diversity of arthropods. Environ Entomol 36: 1254-1268.
62. Schmidt JEU, Braun CU, Whitehouse LP, Hilbeck A (2009) Effects of activated Bt transgene products (Cry1Ab, Cry3Bb) on immature stages of the ladybird Adalia bipunctata in laboratory ecotoxicity testing. Arch Environ Contam Toxicol 56: 221-228.
63. US EPA (2001) Biopesticide registration action document: Bacillus thuringiensis (Bt) plant-incorporated protectants. US Environmental Protection Agency, Washington, DC. http://www. epa. gov/pesticides/biopesticides/pips/bt_brad. htm. Accessed 6 July 2010.
64. US EPA (2003) Biopesticides registration action document: Event MON863 Bacillus thuringiensis Cry3Bb1 corn. US Environmental Protection Agency, Washington, DC. http://cera-gmc. org/docs/decdocs/07-156-003. pdf. Accessed 6 July 2010.
65. US EPA (2007) Biopesticides registration action document. Bacillus thuringiensis Cry3Bb1 corn. US Environmental Protection Agency, Washington, DC. http://epa. gov/opp00001/biopesticides/ingredients/tech_docs/cry3bb1/1_Cry3Bb1_health_characterization. pdf. Accessed 6 July 2010.
66. van Damme EJM, Allen AK, Peumans WJ (1987) Isolation and characterization of a lectin with exclusive specificity towards mannose from snowdrop (Galanthus nivalis) bulbs. FEBS Lett 215: 140-144.
67. 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): e2118. doi: 10. 1371/journal. pone. 0002118.