A controversy re-visited: Is the coccinellid Adalia bipunctata adversely affected by Bt toxins?

Environmental Sciences Europe

Volumn 24, Issue 2, 2012, Pages

  Hilbeck, Angelika ^a   McMillan, Joanna M ^a   Meier, Matthias ^b   Humbel, Anna ^a   Schläpfer Miller, Juanita ^a   Trtikova, Miluse ^a  

^a ETH ZURICH   (Switzerland)

^b RESEARCH INSTITUTE OF ORGANIC AGRICULTURE FIBL   (Switzerland)

Author keywords

Adalia bipunctata; Bacillus thuringiensis; Ecotoxicity testing; Genetically modified crops; German ban Mon810; Ladybeetles; Nontarget organisms

Indexed keywords

ADALIA BIPUNCTATA; BACILLUS THURINGIENSIS; COCCINELLIDAE; HEXAPODA; OSTRINIA NUBILALIS;

BACTERIUM; BEETLE; BIOLOGICAL CONTROL; BIOPESTICIDE; GENETICALLY MODIFIED ORGANISM; MORTALITY; POLLUTION EXPOSURE; TOXIN;

GERMANY;

EID: 84860158548     PISSN: 21904707     EISSN: 21904715     Source Type: Journal    
DOI: 10.1186/2190-4715-24-10     Document Type: Review

References (44)

1. Schmidt JEU, Braun CU, Whitehouse LP, 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.
2. Hilbeck A, Meier M, Römbke J, Jänsch S, Teichmann H, Tappeser B: Environmental risk assessment of genetically modified plants-concepts and controversies. Environ Sci Eur 2011, 23:13.
3. Dolezel M, Miklau M, Hilbeck A, Otto M, Eckerstorfer M, Heisenberger A, Tappeser B, Gaugitsch H: Scrutinizing the current practice of the environmental risk assessment of GM maize applications for cultivation in the EU. Environ Sci Eur 2011.
4. Hilbeck A, Jänsch S, Meier M, Römbke J: Analysis and validation of present ecotoxicological test methods and strategies for the risk assessment of genetically modified plants. BfN-Skripten 2008, 236:287
5. Bundesamt für Verbraucherschutz BVL: Bekanntmachung eines Bescheides zur Beschränkung des Inverkehrbringens von gentechnisch veränderten Mais der Linie Mon810. 2009 [http://www.bvl.bund.de/SharedDocs/Downloads/08- PresseInfothek/mon-810-bescheid.html].
6. Rauschen S: 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 2010, 19:13-16.
7. Ricroch A, Bergé JB, Kuntz M: Is the German suspension of Mon810 maize cultivation scientifically justified? Transgenic Res 2010, 19:1-12.
8. Alvarez-Alfageme F, Bigler F, Romeis J: Laboratory toxicity studies demonstrating no adverse effects of Cry1Ab and Cry3Bb1 to larvae of Adalia bipunctata (Coleoptera: Coccinellidae): the importance of study design. Transgenic Res 2010, doi: 10.1007/s11248-010-9430-5.
9. de Maagd RA, Bravo A, Crickmore N: How Bacillus thuringiensis has evolved specific toxins to colonize the insect world. Trends Genet 2001, 17:193-199. (Pubitemid 32239538)
10. de Maagd RA, Bravo A, Berry C, Crickmore N, Schnepf HE: Structure, diversity, and evolution of protein toxins from spore-forming entopathogenic bacteria. Annu Rev Genet 2003, 37:409-433. (Pubitemid 38041433)
11. Crespo ALB, Spencer TA, Nekl E, Pusztai-Carey M, Moar WJ, Siegfried BD: Comparison and validation of methods to quantify Cry1Ab toxin from Bacillus thuringiensis for standardization of insect bioassays. App Environ Microbiol 2008, 74:130-135.
12. Anilkumar KJ, Pusztai-Carey M, Moar WJ: Fitness costs associated with Cry1Ac-resistant Helicoverpa zea (Lepidoptera: Noctuidae): a factor countering selection for resistance to Bt cotton? J Econ Entomol 2008, 101:1421-1431.
13. Anilkumar KJ, Rodrigo-Simón A, Ferré J, Pusztai-Carey M, Sivasupramaniam S, Moar WJ: Production and characterization of Bacillus thuringiensis Cry1Ac-resistant cotton bollworm Helicoverpa zea (Boddie). Appl Environ Microbiol 2008, 74:462-469.
14. Pusztai-Carey M, Carey PR, Lessard T, Yaguchi M: Isolation, quantitation, and purification of insecticidal proteins from Bacillus thuringiensis. 1994, U.S. patent 5, 356, 788.
15. Banks CJ: The behaviour of individual coccinellid larvae on plants. Br J Animal Behav 1957, 5:12-24.
16. Hagen KS: Biology and ecology of predaceous Coccinellidae. Annu Rev Entomol 1962, 7:289-326.
17. Hodek I, Honek A: Ecology of Coccinellidae Dordrecht: Kluwer; 1996.
18. R Development Core Team: R: A Language and Environment for Statistical Computing Vienna, Austria: R Foundation for Statistical Computing; 2010.
19. Dhillon MK, Sharma HC: Effects of Bacillus thuringiensis δ-endotoxins Cry1Ab and Cry1Ac on the coccinellid beetle, Cheilomenes sexmaculatus (Coleoptera, Coccinellidae) under direct and indirect exposure conditions. Biocontrol Sci Technol 2009, 19:407-420.
20. Moser SE, Harwood JD, Obrycki JJ: Larval feeding on Bt hybrid and non-Bt corn seedlings by Harmonia axyridis (Coleoptera: Coccinellidae) and Coleomegilla maculata (Coleoptera: Coccinellidae). Environ Entomology 2008, 37:525-533. (Pubitemid 351685364)
21. Waltz E: Under wraps. Are the crop industry's strong-arm tactics and close-fisted attitude to sharing seeds holding back independent research and undermining public acceptance of transgenic crops? Nat Biotechnol 2009, 27:880-882
22. US Environmental Protection Agency Office of Pesticide Programs: Biopesticide registration action document: Bacillus thuringiensis Cry34Ab1 and Cry35Ab1 proteins and the genetic material necessary for their production in event DAS-59122-7 corn.[http://www.epa.gov/oppbppd1/biopesticides/ingredients/ tech-docs/brad-006490.pdf]
23. US Environmental Protection Agency Office of Pesticide Programs: Biopesticide registration action document: Bacillus thuringiensis Cry1F corn.[http://www.epa.gov/oppbppd1/biopesticides/ingredients/tech-docs/ brad-006481.pdf].
24. Charleston DS, Dicke M: Designing experimental protocols to investigate the impact of GM crops on non-target arthropods.[http://www.cogem. net/index.cfm/en/publications/publicatie/designing-experimental-protocols-to- investigate-the-impact-of-gm-crops-on-non-target-arthropods].
25. Watanabe PG, Young JD, Gehring PJ: The importance of non-linear (dose-dependent) pharmacokinetics in hazard assessment. J Environ Pathol Toxicol 1977, 1:147-159.
26. Hilbeck A, Schmidt JEU: Another view on Bt-proteins-how specific are they and what else might they do? Biopesticides Int 2006, 2:1-50.
27. Raps A, Kehr J, Gugerli P, Moar WJ, Bigler F, Hilbeck A: Immunological analysis of phloem sap of Bacillus thuringiensis corn and of the nontarget herbivore Rhopalosiphum padi (Homoptera: Aphididae) for the presence of Cry1Ab. Mol Ecol 2001, 10:525-533. (Pubitemid 32232357)
28. Pilcher CD, Obrycki JJ, Rice ME, Lewis LC: Preimaginal development, survival and field abundance of insect predators on transgenic Bacillus thuringiensis corn. Environ Entomol 1997, 26:446-454. (Pubitemid 127478395)
29. Pilcher CD, Rice ME, Obrycki JJ: Impact of transgenic Bacillus thuringiensis corn and crop phenology on five nontarget arthropods. Environ Entomol 2005, 34:1302-1316. (Pubitemid 41434326)
30. Sisterson MS, Biggs RW, Olson C, Carrière Y, Dennehy TJ, Tabashnik BE: Arthropod abundance and diversity in Bt and non-Bt cotton fields. Environ Entomol 2004, 33:921-929. (Pubitemid 39147649)
31. Marvier M, McCreedy C, Regetz J, Kareiva P: A meta-analysis of effects of Bt cotton and maize on non-target invertebrates. Science 2007, 316:1475-1477. (Pubitemid 46906613)
32. Naranjo SE: Impacts of Bt crops on non-target invertebrates and insecticide use patterns. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 2009, 4:1-11.
33. Holmes EE, Kareiva PM: Using single-species measurements to anticipate community level effects of environmental contaminants. In Environmental Contaminants and Terrestrial Vertebrates: Effects on Populations, Communities, and Ecosystems. Edited by: Albers PH, Heinz GH, Ohlendorf HM. Florida: Society of Environmental Toxicology and Chemistry (SETAC); 2000:315.
34. Hilbeck A, Moar W, Pusztai-Carey M, Filipini A, Bigler F: Prey-mediated effects of Cry1Ab toxin and protoxin and Cry2A protoxin on the predator Chrysoperla carnea (Neuroptera: Chrysopidae). Entomol Exp Appl 1999, 91:305-316. (Pubitemid 29422953)
35. Hilbeck A, M Baumgartner M, Fried PM, Bigler: Effects of transgenic Bt corn-fed prey on immature development of Chrysoperla carnea (Neuroptera: Chrysopidae). Environ Entomol 1998, 27:480-487. (Pubitemid 128485667)
36. Hilbeck A, Moar W, Pusztai-Carey M, Filipini A, Bigler F: Toxicity of Bacillus thuringiensis Cry1Ab toxin to the predator Chrysoperla carnea (Neuroptera: Chrysopidae). Environ Entomol 1998, 27:1255-1263. (Pubitemid 128482924)
37. Bohn T, Primicerio R, Hessen DO, Traavik T: Reduced fitness of Daphnia magna fed a Bt-transgenic maize variety. Arch Environ Contam Toxicol 2008, 55:584-592.
38. Rosi-Marshall EJ, Tank JL, Royer RV, Whiles MR, Evans-White M, Chambers C, Griffiths NA, Pokelsek J, Stephens ML: Toxins in transgenic crop byproducts may affect headwater stream ecosystems. Proc Natl Acad Sci USA 2007, 104:16204-16208. (Pubitemid 350099385)
39. Pardo-Lopez L, Munoz-Garay C, Porta H, Rodriguez-Almazan C, Soberon M, Bravo A: Strategies to improve the insecticidal activity of Cry toxins from Bacillus thuringiensis. Peptides 2009, 30:589-595.
40. Graf J: Shifting paradigm on Bacillus thuringiensis toxin and a natural model for Enterococcus faecalis septicaemia. mBio 2011, 2:e00161-11.
41. Broderick NA, Raffa KF, Handelsman J: Midgut bacteria required for Bacillus thuringiensis insecticidal activity. Proc Natl Acad Sci USA 2006, 103:15196-15199. (Pubitemid 44583187)
42. Mason KL, Stepien TA, Blum JE, Holt JF, Labbe NH, Rush JS, Raffa KF, Handelsman J: From commensal to pathogen: translocatoin of Enterococcus faecalis from the midgut to the hemocoel of Manduca sexta. mBio 2011, 2:e00065-11.
43. Kramarz PE, de Vaufleury A, Zygmunt PMS, Verdun C: Increased response to cadmium and Bacillus thuringiensis maize toxicity in the snail Helix aspersa infected by the nematode Phasmarhabditis hermaphrodita. Environ Toxicol Chem 2007, 26:73-79. (Pubitemid 46174376)
44. Van Frankenhuyzen K: Insecticidal activity of Bacillus thuringiensis crystal proteins. J Invertebr Pathol 2009, 101:1-16.