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Assessment of the potential impact of a Bt maize hybrid expressing Cry3Bb1 on ground beetles (Carabidae)

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Abstract

The potential impact of a Bt maize hybrid expressing the coleopteran specific Cry3Bb1 on non-target organisms was assessed in a field release experiment. The study examined the relative abundance of ground beetles (Carabidae) in four maize varieties including the genetically engineered DKC 5143-Bt (event MON 88017), its near-isogenic line DKC 5143 and the two conventional varieties DK 315 and Benicia. Pitfall traps were used to collect the ground dwelling arthropods, which were analyzed to species level. Statistical comparisons showed no significant differences of ground beetle activity densities and diversity patterns between the Bt maize and the near isoline. The internal contents of the Bt protein Cry3Bb1 in ground beetles collected from the field were measured with ELISA. The Bt protein was found in 47% of the ground beetles sampled in Bt plots before the anthesis and in 66% of the individuals sampled after the beginning of maize anthesis.

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References

  • Ahmad A, Wilde GE, Whitworth RJ & Zolnerowich G, 2006. Effect of Corn Hybrids Expressing the Coleopteran-Specific Cry3Bb1 Protein for Corn Rootworm Control on Above-ground Insect Predators. J Econ Entomol 99, 1085–1095.

    Article  CAS  PubMed  Google Scholar 

  • Albajes Garcia R, Farinós GP, Pérez-Hedo M, Poza M de la Lumbierres B, Ortego F, Pons X & Castañera P, 2012. Post-market environmental monitoring of Bt maize in Spain: Non-target effects of varieties derived from the event MON810 on predator y fauna. Span J Agric Res 10, 977–985.

    Article  Google Scholar 

  • Alvarez-Alfageme F, Ortego F & Castanera P, 2009. Bt maize fed-prey mediated effect on fitness and digestive physiology of the ground predator Poecilus cupreus L. (Coleoptera: Carabidae). J Insect Physiol 55, 144–150.

    Article  Google Scholar 

  • Bhatti MA, Duan J, Head G, 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 Ground-Dwelling Invertebrates. Environ. Entomol. 34, 1325–1335.

    Article  Google Scholar 

  • Carrière Y, Ellers-Kirk C, Sisterson M, Antilla L, Whitlow M, Dennehy TJ & Tabashnik BE, 2003. Long-term regional suppression of pink bollworm by Bacillus thuringiensis cotton. Proc Natl Acad Sci 100, 1519–1523.

    Article  PubMed  PubMed Central  Google Scholar 

  • Daly T & Buntin GD, 2005. Effect of Bacillus thuringiensis Transgenic Corn for Lepidopteran Control on Nontarget Arthropods. Environ Entomol 34, 1292–1301.

    Article  Google Scholar 

  • Efron B & Tibshirani RJ, 1993. An Introduction to the Bootstrap. Chapman and Hall, New York.

    Book  Google Scholar 

  • European Commission, 2001. Directive 2001/18/EC of the European Parliament and of the Council of 12 March 2001 on the deliberate release into the environment of genetically modified organisms and repealing Council Directive 90/220/EEC. L 106/1 of 4/17/2001.

    Google Scholar 

  • European Commission, 2003. Regulation (EC) 1829/2003 of the European Parliament and of the Council of 22 September 2003 on genetically modified food and feed. L 268/1 of 10/18/2003.

    Google Scholar 

  • Farinós GP, Poza de la M, Hernández-Crespo P, Ortego F & Castañera P, 2008. Diversity and seasonal phenology of aboveground arthropods in conventional and transgenic maize crops in Central Spain. Biological Control 44, 362–371.

    Article  Google Scholar 

  • Ferry N, Mulligan EA, Majerus MEN & Gatehouse AMR, 2007. Bitrophic and tritrophic effects of Bt Cry3A transgenic potato on beneficial, nontarget, beetles. Transgenic Res 16, 795–812.

    Article  CAS  PubMed  Google Scholar 

  • Harwood JD, Samson RA & Obrycki JJ, 2006. No evidence for the uptake of Cry1Ab Bt-endotoxins by the generalist predator Scarites subterraneus (Coleoptera: Carabidae) in laboratory and field experiments. Biocontrol Sci Tec 16, 377–388.

    Article  Google Scholar 

  • Helenius J, Holopainen JK, Huusela-Veistola E, Kurppa S, Pokki P & Varis A, 2001. Ground beetle (Coleotera: Cara-bidae) diversity in Finnish arable land. Agr food sci Finland 10, 261–276.

    Google Scholar 

  • Holland JM, Winder L & Perry JN, 2000. The impact of dimethoate on the spatial distribution of bene cial arthropods. Ann Appl Biol 136, 93–105.

    Article  CAS  Google Scholar 

  • Holopainen JK, Berman T, Hautala E-L & Oksanen J, 1995. The ground beetle fauna (Coleoptera: Carabidae) in relation to soil properties and foliar fluoride content in spring cereals. Pedobiologia 39, 193–206.

    Google Scholar 

  • James C, 2012. Global Status of Commercialized Biotech/GM Crops: 2012. ISAAA Brief No. 44. ISAAA: Ithaca, NY.

    Google Scholar 

  • Köhler F & Klausnitzer B, 1998. Verzeichnis der Käfer Deutschlands. Entomol Nachr Ber (Dresden) Beiheft 4, 1–185.

    Google Scholar 

  • Kromp B, 1999. Carabid beetles in sustainable agriculture: a review on pest control efficacy, cultivation impacts and enhancement. Agr Ecosyst Environ 74, 187–228.

    Article  Google Scholar 

  • Kuhar TP, Youngman RR & Laub CA, 1997. Risk of western corn rootworm (Coleoptera: Chrysomelidae) damage to continuous corn in Virginia. J Entomol Sci 32, 281–289.

    Google Scholar 

  • Leslie TW, Biddinger DJ, Mullin CA & Fleischer SJ, 2009. Carabidae Population Dynamics and Temporal Partitioning: Response to Coupled Neonicotinoid-transgenic Technologies in Maize. Environ Entomol 38, 935–943.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Lundgren JG, Gassmann AJ, Bernal J, Duan JJ & Ruberson J, 2009. Ecological compatibility of GM crops and biological control. Crop Prot 28, 1017–1030.

    Article  Google Scholar 

  • Lutz B, Wiedemann S, Einspanier R, Mayer J & Albrecht C, 2005. Degradation of Cry1Ab-protein from genetically modified maize in the bovine gastrointestinal tract. J Agr Food Chem 53, 1453–1456.

    Article  CAS  Google Scholar 

  • Magurran AE, 2004. Measuring Biological Diversity. Black-well Publishing, Malden, MA, USA.

    Google Scholar 

  • McCulloch CE & Searle SR, 2001. Generalized, linear, and mixed models. Wiley, Hoboken.

    Google Scholar 

  • Meissle M, Vojtech E & Poppy GM, 2005. Effects of Bt maize-fed prey on the generalist predator Poecilus cupreus L. (Coleoptera: Carabidae). Transgenic Res 14, 123–132.

    Article  CAS  PubMed  Google Scholar 

  • Miller N, Estoup A, Toepfer S, Bourguet D, Lapchin L, Derridj S, Kim KS, Reynaud P, Furlan L & Guillemaud T, 2005. Multiple Transatlantic Introductions of the Western Corn Rootworm. Science 310, 992.

    Article  CAS  PubMed  Google Scholar 

  • Monsanto Company, 2003. Application for authorization of MON 88017 maize in the European Union, according to Regulation (EC) No 1829/2003 on genetically modified food and feed: 10.

    Google Scholar 

  • Müller-Motzfeld G, 2004. Die Käfer Mitteleuropas, Bd. 2: Adephaga I: Carabidae. 2. Auflage. Elsevier.

    Google Scholar 

  • Mullin CA, Saunders MC II, Leslie TW, Biddinger DJ & Fleischer SJ, 2005. Toxic and Behavioral Effects to Cara-bidae of Seed Treatments Used on Cry3Bb1- and Cry1Ab/ c-Protected Corn. Environ Entomol 34, 1626–1336.

    Article  CAS  Google Scholar 

  • Perry JN, ter Braak CJF, Dixon PM, Duan JJ, Hails RS, Huesken A, Lavielle M, Marvier M, Scardi M, Schmidt K, Tothmeresz B, Schaarschmidt F & van der Voet H, 2009. Statistical aspects of environmental risk assessment of GM plants for effects on non-target organisms. Environ Biosafety Res 8, 65–78.

    Article  PubMed  Google Scholar 

  • Peterson JA, Obrycki JJ & Harwood JD, 2009. Quantification of Bt-endotoxin exposure pathways in carabid food webs across multiple transgenic events. Biocontrol Sci Techn 19, 613–625.

    Article  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, 2008. Assessment of risk of insect-resistant transgenic crops to nontarget arthropods. Nat Biotechnol 26, 203–208.

    Article  CAS  PubMed  Google Scholar 

  • Szekeres D & Kádár F & Kiss J, 2006. Activity density, diversity and seasonal dynamics of ground beetles (Coleoptera: Carabidae) in Bt- (MON810) and in isogenic maize stands. Entomol Fennica 17, 269–275.

    Google Scholar 

  • Thomas CFG, Holland JM & Brown NJ, 2002. The Spatial Distribution of Carabid Beetles in Agricultural Landscapes. In: The Agroecology of Carabid Beetles. Ed. by Holland JM, Intercept, Andover, UK, 305–344.

    Google Scholar 

  • Tischler W, 1965. Agrarökologie. VEB Gustav Fischer Verlag, Jena, 150–160.

    Google Scholar 

  • Toft S & Bilde T, 2002. Carabid diets and food value. In: The Agroecology of Carabid Beetles. Ed. by Holland JM, Intercept, Andover, UK, 81–110.

    Google Scholar 

  • Toschki A, Hothorn LA & Roß-Nickoll M, 2007. Effects of Cultivation of Genetically Modified Bt maize on Epigeic Arthropods (Araneae; Carabidae). Environ Entomol 36, 967–981.

    Article  CAS  PubMed  Google Scholar 

  • Venables WN & Ripley BD, 2002. Modern Applied Statistics with S. Fourth Edition. Springer-Verlag, New York.

    Book  Google Scholar 

  • Volkmar C, Lübke-Al Hussein M, Jany D, Hunold I, Richter L, Kreuter T & Wetzel T, 2002. Ecological studies on epigeous arthropod populations of transgenic sugar beet at Friemar (Thuringia, Germany) Agr Ecosyst Environ 95, 37–47.

    Article  Google Scholar 

  • Zwahlen C & Andow DA, 2005. Field evidence for the exposure of ground beetles to Cr y1Ab from transgenic corn. Env Biosafety Res 4, 113–117.

    Article  CAS  Google Scholar 

Download references

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Correspondence to Kai U. Priesnitz.

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Priesnitz, K.U., Benker, U. & Schaarschmidt, F. Assessment of the potential impact of a Bt maize hybrid expressing Cry3Bb1 on ground beetles (Carabidae). J Plant Dis Prot 120, 131–140 (2013). https://doi.org/10.1007/BF03356464

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