Skip to main content
SpringerLink
Log in

Non-target organism effects tests on Vip3A and their application to the ecological risk assessment for cultivation of MIR162 maize

  • Original Paper
  • Published:
Transgenic Research Aims and scope Submit manuscript

Abstract

Transgenic crops producing insecticidal proteins from Bacillus thuringiensis (Bt) provide economic, environmental and health benefits by maintaining or increasing crop yields with fewer applications of insecticide. To sustain these benefits, it is important to delay the evolution of insect resistance to the proteins, and to ensure that the proteins do not harm non-target organisms, particularly those that may control secondary pests that would otherwise flourish because of reduced insecticide applications. Vip3A is a Bt vegetative insecticidal protein that is active against lepidopterous pests. It has a different mode of action from other proteins for control of Lepidoptera in current Bt crops, and when combined with these proteins, it should help to delay the evolution of pest resistance to Bt crops. This paper presents data on the effects of Vip3A on non-target organisms, and an ecological risk assessment of MIR162 maize, which expresses Vip3Aa20. Laboratory studies indicate few adverse effects of Vip3A to non-target organisms: 11 of 12 species tested showed no adverse effects when exposed to high concentrations of Vip3A relative to estimated exposures resulting from cultivation of MIR162 maize. Daphnia magna exposed to Vip3Aa20 were unaffected in terms of survival or fecundity, but grew slightly more slowly than unexposed controls. The data indicate that cultivation of MIR162 maize poses negligible risk to non-target organisms, and that crops producing Vip3A are unlikely to adversely affect biological control organisms such that benefits from reduced insecticide applications are lost.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Notes

  1. Event Pacha maize was not commercialised and was superseded by MIR162 maize.

References

  • Adamczyk JJ Jr, Adams LC, Hardee DD (2001) Field efficacy and seasonal expression profiles for terminal leaves of single and double Bacillus thuringiensis toxin cotton genotypes. J Econ Entomol 94:1589–1593

    Article  PubMed  CAS  Google Scholar 

  • Agaisse H, Lereclus D (1995) How does Bacillus thuringiensis produce so much insecticidal crystal protein? J Bacteriol 177:6027–6032

    PubMed  CAS  Google Scholar 

  • Armstrong CL, Parker GB, Pershing JC, Brown SM, Sanders PR, Duncan DR, Stone T, Dean DA, DeBoer DL, Hart J (1995) Field evaluation of European corn borer control in progeny of 173 transgenic crop events expressing an insecticidal protein from Bacillus thuringiensis. Crop Sci 35:550–557

    Article  Google Scholar 

  • Babendreier D, Kalberer N, Romeis J, Fluri P, Bigler F (2004) Pollen consumption in honey bee larvae: a step forward in the risk assessment of transgenic plants. Apidologie 35:293–300

    Article  Google Scholar 

  • Bakker FM, Aldershof SA, van der Veire M, Candolfi MP, Izquierdo JI, Kleiner R, Neumann Ch, Nienstedt KM, Walker H (2000) A laboratory test for evaluating the effects of plant protection products on the predatory bug, Orius laevigatus (Fieber) (Heteroptera: Anthocoridae). In: Candolfi MP, Blumel S, Forster R, Bakker FM, Grimm C, Hassan SA, Heimbach U, Mead-Briggs MA, Reber B, Schmuck R, Vogt H (eds) Guidelines to evaluate side-effects of plant protection products to non-target arthropods. IOBC/WPRS, Gent, pp 57–70

    Google Scholar 

  • Bates SL, Zhao J-Z, Roush RT, Shelton AM (2005) Insect resistance management in GM crops: past, present and future. Nat Biotechnol 23:57–62

    Article  PubMed  CAS  Google Scholar 

  • Brookes G, Barfoot P (2008) Global impact of biotech crops: socio-economic and environmental effects 1996–2006. AgBioForum 11:21–38

    Google Scholar 

  • Buikema AL Jr, Geiger JG, Lee DR (1980) Daphnia toxicity tests. In: Buikema AL, Cairns J (eds) Aquatic invertebrate bioassays. American Society for Testing and Materials, Philadelphia, pp 48–69

    Chapter  Google Scholar 

  • Campbell PJ, Brown KC, Harrison EG, Bakker F, Barrett KL, Candolfi MP, Cañez V, Dinter A, Lewis G, Mead-Briggs M, Miles M, Neumann P, Romijn K, Schmuck R, Shires S, Ufer A, Waltersdorfer A (2000) A hazard-quotient approach for assessing the risk to non-target arthropods from plant protection products under 91/414/EEC: hazard quotient trigger value proposal and validation. J Pest Sci 73:117–124

    Google Scholar 

  • Carpenter JE (2010) Peer-reviewed surveys indicate positive impact of commercialized GM crops. Nat Biotechnol 28:319–321

    Article  PubMed  CAS  Google Scholar 

  • Crocker D, Hart A, Gurney J, McCoy C (2002) Project PN0908: methods for estimating daily food intake of wild birds and mammals. Central Science Laboratory. Unpublished report to the (UK) Department for Environment, Food and Rural Affairs. Available at http://www.pesticides.gov.uk/uploadedfiles/Web_Assets/PSD/Research_PN0908.pdf

  • Dale PJ, Clarke B, Fontes EMG (2002) Potential for the environmental impact of transgenic crops. Nat Biotechnol 20:567–574

    Article  PubMed  CAS  Google Scholar 

  • Dively G (2005) Impact of transgenic VIP3A x Cry1Ab lepidopteran-resistant field corn on the nontarget arthropod community. Environ Entomol 34:1267–1291

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Ecobichon DJ (2001) Pesticide use in developing countries. Toxicol 160:27–33

    Article  CAS  Google Scholar 

  • Ellis BA, Mills JN, Glass GE, McKee KT, Enria DA, Childs JE (1998) Dietary habits of the common rodents in an agroecosystem in Argentina. J Mammal 79:1203–1220

    Article  Google Scholar 

  • Estruch JJ, Warren GW, Mullins MA, Nye GJ, Craig JA, Koziel MG (1996) Vip3A, a novel Bacillus thuringiensis vegetative insecticidal protein with a wide spectrum of activities against lepidopteran insect. Proc Natl Acad Sci USA 93:5389–5394

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Alonso M, Jacobs E, Raybould A, Nickson TE, Sowig P, Willekens H, van der Kouwe P, Layton R, Amijee F, Fuentes A, Tencalla F (2006) A tiered system for assessing the risk of genetically modified plants to non-target organisms. Environ Biosafety Res 5:57–65

    Article  PubMed  Google Scholar 

  • Grimm C, Reber B, Barth M, Candolfi MP, Drexler A, Maus C, Moreth L, Ufer A, Walterdorfer A (2000) A test for evaluating the chronic effects of plant protection products on the rove beetle Aleochara bilineata Gyll. (Coleoptera: Staphylinidae) under laboratory and extended laboratory conditions. In: Candolfi MP, Blumel S, Forster R, Bakker FM, Grimm C, Hassan SA, Heimbach U, Mead-Briggs MA, Reber B, Schmuck R, Vogt H (eds) Guidelines to evaluate side-effects of plant protection products to non-target arthropods. IOBC/WPRS, Gent, pp 1–10

    Google Scholar 

  • Herman RA, Chassy BM, Parrott W (2009) Compositional assessment of transgenic crops: an idea whose time has passed. Trends Biotechnol 27:555–557

    Article  PubMed  CAS  Google Scholar 

  • Homan HJ, Linz GM, Bleier WJ (1994) Effect of crop phenology and habitat on the diet of common grackles (Quiscalus quiscula). Am Midl Nat 131:381–385

    Article  Google Scholar 

  • Houtcooper WC (1978) Food habits of rodents in a cultivated ecosystem. J Mammal 59:427–430

    Article  Google Scholar 

  • Huang J, Hu R, Pray C, Qiao F, Rozelle S (2003) Biotechnology as an alternative to chemical pesticides. Agric Econ 29:55–67

    Article  Google Scholar 

  • Jackson RE, Marcus MA, Gould F, Bradley JR, Van Duyn JW (2007) Cross-resistance responses of Cry1Ac-selected Heliothis virescens (Lepidoptera: Noctuidae) to the Bacillus thuringiensis protein Vip3A. J Econ Entomol 100:180–186

    Article  PubMed  CAS  Google Scholar 

  • Jaffe G (2004) Regulating transgenic crops: a comparative analysis of different regulatory processes. Transgenic Res 13:5–19

    Article  PubMed  CAS  Google Scholar 

  • Janmaat AF, Myers J (2003) Rapid evolution and the cost of resistance to Bacillus thuringiensis in greenhouse populations of cabbage loopers, Trichoplusia ni. Proc R Soc Lond B 270:2263–2270

    Article  Google Scholar 

  • Kos M, van Loon JJA, Dicke M, Vet LEM (2009) Transgenic plants as vital components of integrated pest management. Trends Biotechnol 27:621–627

    Article  PubMed  CAS  Google Scholar 

  • Kurtz RW, McCaffery A, O’Reilly D (2007) Insect resistance management for Syngenta’s VipCotTM transgenic cotton. J Invert Pathol 95:227–230

    Article  Google Scholar 

  • Lee MK, Walters FS, Hart H, Palekar N, Chen J-S (2003) The mode of action of the Bacillus thuringiensis vegetative insecticidal protein Vip3A differs from that of the Cry1Ab δ-endotoxin. Appl Environ Microbiol 69:4648–4657

    Article  PubMed  CAS  Google Scholar 

  • Lee MK, Miles P, Chen J-S (2006) Brush border membrane binding properties of Bacllus thuringiensis Vip3A toxin to Heliothis virescens and Helicoverpa zea midguts. Bichem Biophys Res Commun 339:1043–1047

    Article  CAS  Google Scholar 

  • Lipton CR, Dautlick JX, Grothaus GD, Hunst PL, Magin KM, Mihaliak CA, Rubio FM, Stave JW (2000) Guidelines for the validation and use of immunoassays for the determination of introduced proteins in biotechnology enhanced crops and derived food ingredients. Food Agric Immunol 12:153–164

    Article  CAS  Google Scholar 

  • Lu YH, Qiu F, Feng HQ, Li HB, Yang ZC, Wyckhuys KAG, Wu KM (2008) Species composition and seasonal abundance of pestiferous plant bugs (Hemiptera: Miridae) on Bt cotton in China. Crop Prot 27:465–472

    Article  Google Scholar 

  • Lu Y, Wu K, Jiang Y, Xia B, Li P, Feng H, Wyckhuys KAG, Guo Y (2010) Mirid bug outbreaks in multiple crops correlated with wide-scale adoption of Bt cotton in China. Science 328:1151–1154

    Article  PubMed  CAS  Google Scholar 

  • Marvier M, McCreedy C, Regetz J, Kareiva P (2007) A meta-analysis of effects of Bt cotton and maize on non-target invertebrates. Science 316:1475–1477

    Article  PubMed  CAS  Google Scholar 

  • Metcalf RL (1980) Changing role of insecticides in crop protection. Ann Rev Entomol 25:219–256

    Article  CAS  Google Scholar 

  • Morse S, Bennett RM, Ismael Y (2005) Genetically modified insect resistance in cotton: some farm level economic impacts in India. Crop Prot 24:433–440

    Article  Google Scholar 

  • Naranjo S (2009) Impacts of Bt crops on non-target invertebrates and insecticide use patterns. CAB Rev Perspect Agric Vet Sci Nutrit Nat Resour 4:1–23

    Google Scholar 

  • Newsom LD (1967) Consequences of insecticide use on nontarget organisms. Ann Rev Entomol 12:257–286

    Article  CAS  Google Scholar 

  • NRC (National Research Council) (1983) Nutrient requirements of warmwater fishes and shellfishes. National Academy Press, Washington, DC

    Google Scholar 

  • Oomen PA, de Ruijter A, van der Steen J (1992) Method for honeybee brood feeding tests with insect growth-regulating insecticides. EPPO Bull 22:613–616

    Article  Google Scholar 

  • Ostry V, Ovesna J, Skarkova J, Pouchova V, Ruprich J (2010) A review on comparative data concerning Fusarium mycotoxins in Bt maize and non-Bt isogenic maize. Mycotoxin Res. doi: 10.1007/s12550-010-0056-5

  • Qaim M, Pray CE, Zilberman D (2008) Economic and social considerations in the adoption of Bt crops. In: Romeis J, Shelton AM, Kennedy GG (eds) Integration of insect-resistant genetically modified crops within IPM programs. Springer, New York, pp 329–356

    Chapter  Google Scholar 

  • Raney T (2006) Economic impact of transgenic crops in developing countries. Curr Opin Plant Biol 17:1–5

    Google Scholar 

  • Raybould A, Stacey D, Vlachos D, Graser G, Li X, Joseph R (2007) Non-target organism risk assessment of MIR604 maize expressing mCry3A for control of corn rootworm. J Appl Entomol 131:391–399

    Article  CAS  Google Scholar 

  • Raybould A, Tuttle A, Shore S, Stone T (2010) Environmental risk assessments for transgenic crops producing output trait enzymes. Transgenic Res. doi: 10.1007/s11248-009-9343-3

  • Romeis J, Meissle M, Bigler F (2006) Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nat Biotechnol 24:63–71

    Article  PubMed  CAS  Google Scholar 

  • 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 (2008a) Assessment of risk of insect-resistant transgenic crops to nontarget arthropods. Nat Biotechnol 26:203–208

    Article  PubMed  CAS  Google Scholar 

  • Romeis J, Van Driesche RG, Barrett BIP, Bigler F (2008b) Insect-resistant transgenic crops and biological control. In: Romeis J, Shelton AM, Kennedy GG (eds) Integration of insect-resistant genetically modified crops within IPM programs. Springer, New York, pp 87–117

    Chapter  Google Scholar 

  • Shelton AM, Zhao J-Z, Roush RT (2002) Economic, ecological, food safety, and social consequences of the deployment of Bt transgenic plants. Ann Rev Entomol 47:845–881

    Article  CAS  Google Scholar 

  • Tabashnik BE, Cushing NL, Finson N, Johnson MW (1990) Field development of resistance to Bacillus thuringiensis in diamondback moth (Lepidoptera: Plutellidae). J Econ Entomol 83:1671–1676

    Google Scholar 

  • USEPA (United States Environmental Protection Agency) (2004) Dichlormid: time-limited pesticide tolerances. Fed Reg 69:58285–58290

    Google Scholar 

  • USEPA (United States Environmental Protection Agency) (2008) Biopesticides registration action document. Bacillus thuringiensis modified Cry1Ab (SYN-IR67B-1) and Vip3Aa19 (SYN-IR102-7) insecticidal proteins and the genetic material necessary for their production in COT102 X COT67B cotton. Available at http://www.epa.gov/pesticides/biopesticides/ingredients/tech_docs/brad_006529.pdf

  • USEPA (United States Environmental Protection Agency) (2009) Biopesticides registration action document. Bacillus thuringiensis Vip3Aa20 insecticidal protein and the genetic material necessary for its production (via elements of vector pNOV1300) in Event MIR162 maize (OECD unique identifier: SYN-IR162-4). Available at http://www.epa.gov/oppbppd1/biopesticides/ingredients/tech_docs/brad_006599.pdf

  • Vogt H, Bigler F, Brown K, Candolfi MP, Kemmeter F, Kühner Ch, Moll M, Travis A, Ufer A, Viñuela E, Waldburger M, Waltersdorfer A (2000) Laboratory method to test effects of plant protection products on larvae of Chrysoperla carnea (Neuroptera: Chrysopidae). In: Candolfi MP, Blümel R, SR Forster, FM Bakker, Grimm C, Hassan SA, Heimbach U, Mead-Briggs MA, Reber B, Schmuck R, Vogt H (eds) Guidelines to evaluate side-effects of plant protection products to non-target arthropods. IOBC/WPRS, Gent, pp 27–44

    Google Scholar 

  • Whitehouse MEA, Wilson LJ, Constable GA (2007) Target and non-target effects on the invertebrate community of Vip cotton, a new insecticidal transgenic. Aust J Agric Res 58:273–285

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank the many scientists who directed studies summarised in this paper: Gerson Graser, Cheryl Stacy, Kim Hill, Catherine Kramer, Laura Privalle, David Stacey, Robin Blake and Emma Barnes at Syngenta; Mark Cafarella, Arthur Putt and Deb Teixeira at Springborn Smithers Laboratories; and Stephen Vinall at Mambo-Tox Ltd.

Author information

Authors and Affiliations

  1. Syngenta, Jealott’s Hill International Research Centre, Bracknell, Berkshire, RG22 4JN, UK

    Alan Raybould

  2. Syngenta Biotechnology, Inc., 3054 East Cornwallis Road, Post Office Box 12257, Research Triangle Park, NC, 27709, USA

    Demetra Vlachos

Authors
  1. Alan Raybould
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Demetra Vlachos
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alan Raybould.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Raybould, A., Vlachos, D. Non-target organism effects tests on Vip3A and their application to the ecological risk assessment for cultivation of MIR162 maize. Transgenic Res 20, 599–611 (2011). https://doi.org/10.1007/s11248-010-9442-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11248-010-9442-1

Keywords

Search

Navigation