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Sensitivity of the cereal leaf beetle Oulema melanopus (Coleoptera: Chrysomelidae) to Bt maize-expressed Cry3Bb1 and Cry1Ab

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Abstract

The sensitivity of the cereal leaf beetle, Oulema melanopus (Coleoptera: Chrysomelidae), to maize-expressed Bacillus thuringiensis (Bt) proteins was investigated in the present study. Neonate larvae of O. melanopus were caged on leaves of Cry3Bb1-expressing (MON88017) or Cry1Ab-expressing (MON810) Bt maize, the corresponding near-isolines, or two non-related, conventional maize varieties. Larval survival was reduced on Cry3Bb1-expressing, but not on Cry1Ab-expressing maize compared with conventional varieties. Differences among conventional varieties were also present. The amount of eaten leaf material, developmental time to prepupal stage, and prepupal weight did not differ between Bt maize varieties and their corresponding near-isolines. In an additional feeding study with newly emerged adults, survival and beetle weight did not differ when leaves of Cry3Bb1-expressing maize or the near-isoline were offered as food over 3 weeks. ELISA measurements revealed that larvae feeding on Bt maize contained rather high Cry3Bb1 or Cry1Ab levels, which were in the same order of magnitude as the leaves. In contrast, concentrations in feces were one order, and concentrations in prepupae and adults two orders of magnitude lower.

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References

  • Álvarez-Alfageme F, Bigler F, Romeis J (2011) Laboratory toxicity studies demonstrate no adverse effects of Cry1Ab and Cry3Bb1 to larvae of Adalia bipunctata (Coleoptera: Coccinellidae): the importance of study design. Transgenic Res 20:467–479

    Article  PubMed  Google Scholar 

  • Bhatti MA, Duan J, Head GP, Jiang CJ, 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

    Article  Google Scholar 

  • CERA (2011) GM Crop database. Center for environmental risk assessment (CERA), ILSI Research Foundation, Washington D.C. http://cera-gmc.org/index.php?action=gm_crop_database. Accessed 28 Oct 2011

  • Donovan WP, Rupar MJ, Slaney AC, Malvar T, Gawronburke MC, Johnson TB (1992) Characterization of two genes encoding Bacillus thuringiensis insecticidal crystal proteins toxic to Coleoptera species. Appl Environ Microbiol 58:3921–3927

    PubMed  CAS  Google Scholar 

  • Duan JJ, Marvier M, Huesing JE, Dively G, Huang ZY (2008) A meta-analysis of effects of Bt crops on honey bees (Hymenoptera: Apidae). PLoS ONE 3:e1415

    Article  PubMed  Google Scholar 

  • Dutton A, Obrist L, D’Alessandro M, Diener L, Müller M, Romeis J, Bigler F (2004) Tracking Bt-toxin in transgenic maize for risk assessment on non-target arthropods. IOBC/wprs Bulletin 27(3):57–63

    Google Scholar 

  • Dutton A, Romeis J, Bigler F (2005) Effects of Bt maize expressing Cry1Ab and Bt spray on Spodoptera littoralis. Entomol Exp Appl 114:161–169

    Article  CAS  Google Scholar 

  • Felke M, Lorenz N, Langenbruch GA (2002) Laboratory studies on the effects of pollen from Bt-maize on larvae of some butterfly species. J Appl Entomol 126:320–325

    Article  Google Scholar 

  • Glare TR, O’Callaghan M (2000) Bacillus thuringiensis: biology, ecology and safety. Wiley, Chichester

    Google Scholar 

  • Guppy JC, Harcourt DG (1978) Effects of temperature on development of the immature stages of the cereal leaf beetle, Oulema melanopus (Coleoptera: Chrysomelidae). Can Entomol 110:257–263

    Article  Google Scholar 

  • Haynes DL, Gage SH (1981) The cereal leaf beetle in North America. Annu Rev Entomol 26:259–287

    Article  Google Scholar 

  • Hellmich RL, Siegfried BD, Sears MK, Stanley-Horn DE, Daniels MJ, Mattila HR, Spencer T, Bidne KG, Lewis LC (2001) Monarch larvae sensitivity to Bacillus thuringiensis-purified proteins and pollen. Proc Natl Acad Sci USA 98:11925–11930

    Article  PubMed  CAS  Google Scholar 

  • Hill D (1987) Agricultural insect pests of temperate regions and their control. Cambridge University Press, Cambridge

    Google Scholar 

  • Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Statist 6:65–70

    Google Scholar 

  • ICH (2005) Harmonised tripartite guideline: Validation of analytical procedures: text and methodology Q2(R1). International conference on harmonisation of technical requirements for registration of pharmaceuticals for human use. http://www.ich.org/fileadmin/Public_Web_Site/ICH_Products/Guidelines/Quality/Q2_R1/Step4/Q2_R1__Guideline.pdf. Accessed 28 Oct 2011

  • Icoz I, Stotzky G (2008) Fate and effects of insect-resistant Bt crops in soil ecosystems. Soil Biol Biochem 40:559–586

    Article  CAS  Google Scholar 

  • Johnson TB, Slaney AC, Donovan WP, Rupar MJ (1993) Insecticidal activity of EG4961, a novel strain of Bacillus thuringiensis toxic to larvae and adults of southern corn rootworm (Coleoptera: Chrysomelidae) and Colorado potato beetle (Coleoptera: Chrysomelidae). J Econ Entomol 86:330–333

    Google Scholar 

  • Keller B, Langenbruch GA (1993) Control of coleopteran pests by Bacillus thuringiensis. In: Entwistle PF, Cory JS, Bailey MJ, Higgs S (eds) Bacillus thuringiensis, an environmental biopesticide: theory and practice. Wiley, Chichester, pp 171–191

    Google Scholar 

  • Leslie TW, Biddinger DJ, Rohr JR, Fleischer SJ (2010) Conventional and seed-based insect management strategies similarly influence nontarget coleopteran communities in maize. Environ Entomol 39:2045–2055

    Article  PubMed  CAS  Google Scholar 

  • 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 Control 53:337–344

    Article  CAS  Google Scholar 

  • 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 (ed) Proceedings of the third international symposium on biological control of arthropods, Christchurch, New Zealand, 8-13 February 2009, FHTET-2008-06. Morgantown: United States Department of Agriculture, Forest Service, pp 145–160

  • Meissle M, Romeis J (2009a) Insecticidal activity of Cry3Bb1 expressed in Bt maize on larvae of the Colorado potato beetle, Leptinotarsa decemlineata. Entomol Exp Appl 131:308–319

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Meissle M, Pilz C, Romeis J (2009) Susceptibility of Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae) to the entomopathogenic fungus Metarhizium anisopliae when feeding on Bacillus thuringiensis Cry3Bb1-expressing maize. Appl Environ Microbiol 75:3937–3943

    Article  PubMed  CAS  Google Scholar 

  • Meissle M, Hellmich RL, Romeis J (2011) Impact of Cry3Bb1-expressing Bt maize on adults of the western corn rootworm, Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae). Pest Manag Sci 67:1049–1058

    Article  CAS  Google Scholar 

  • Myser WC, Schultz WB (1967) Sexing the adult cereal leaf beetle, Oulema melanopus (Coleoptera: Chrysomelidae). Ann Entomol Soc Am 66:1329

    Google Scholar 

  • 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, vol 4, no. 011

  • Obrist LB, Dutton A, Albajes R, Bigler F (2006) Exposure of arthropod predators to Cry1Ab toxin in Bt maize fields. Ecol Entomol 31:141–154

    Article  Google Scholar 

  • OECD (2007) Consensus document on safety information on transgenic plants expressing Bacillus thuringiensis—derived insect control protein. Series on Harmonisation of Regulatory Oversight in Biotechnology, No. 42. Organisation for Economic Co-operation and Development, Paris

  • Olfert O, Weiss RM, Woods S, Philip H, Dosdall L (2004) Potential distribution and relative abundance of an invasive cereal crop pest, Oulema melanopus (Coleoptera: Chrysomelidae), in Canada. Can Entomol 136:277–287

    Article  Google Scholar 

  • Park Y, Abdullah MAF, Taylor MD, Rahman K, Adang MJ (2009) Enhancement of Bacillus thuringiensis Cry3Aa and Cry3Bb toxicities to coleopteran larvae by a toxin-binding fragment of an insect cadherin. Appl Environ Microbiol 75:3086–3092

    Article  PubMed  CAS  Google Scholar 

  • Rauschen S, Schaarschmidt F, Gathmann A (2010) Occurrence and field densities of Coleoptera in the maize herb layer: implications for environmental risk assessment of genetically modified Bt-maize. Transgenic Res 19:727–744

    Article  PubMed  CAS  Google Scholar 

  • Romeis J, Meissle M (2011) Non-target risk assessment of Bt crops—Cry protein uptake by aphids. J Appl Entomol 135:1–6

    Article  CAS  Google Scholar 

  • 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, Meissle M, Raybould A, Hellmich RL (2009) Impact of insect-resistant transgenic crops on above-ground non-target arthropods. In: Ferry N, Gatehouse AMR (eds) Environmental impact of genetically modified crops. CAB International, Wallingford, pp 165–198

    Chapter  Google Scholar 

  • Shade RE, Wilson MC (1967) Leaf-vein spacing as a factor affecting larval feeding behaviour of the cereal leaf beetle, Oulema melanopus (Coleoptera: Chrysomelidae). Ann Entomol Soc Am 60:493–496

    Google Scholar 

  • Shirai Y (2006) Laboratory evaluation of effects of transgenic Bt corn pollen on two non-target herbivorous beetles, Epilachna vigintioctopunctata (Coccinellidae) and Galerucella vittaticollis (Chrysomelidae). Appl Entomol Zool 41:607–611

    Article  CAS  Google Scholar 

  • Siegfried BD, Vaughn TT, Spencer T (2005) Baseline susceptibility of western corn rootworm (Coleoptera: Chrysomelidae) to Cry3Bb1 Bacillus thuringiensis toxin. J Econ Entomol 98:1320–1324

    Article  PubMed  CAS  Google Scholar 

  • US EPA (2001) Biopesticides registration action document—Bacillus thuringiensis plant-incorporated protectants. United States Environmental Protection Agency. http://www.epa.gov/oppbppd1/biopesticides/pips/bt_brad.htm. Accessed 28 Oct 2011

  • US EPA (2007) Biopesticides registration action document—Bacillus thuringiensis Cry3Bb1 corn. United States Environmental Protection Agency. http://www.epa.gov/pesticides/biopesticides/ingredients/tech_docs/brad_006484.htm. Accessed 28 Oct 2011

  • van Frankenhuyzen K, Nystrom C (2002) The Bacillus thuringiensis toxin specificity database. Last Update 16 Dec 2010. Natural Resources Canada. http://www.glfc.cfs.nrcan.gc.ca/bacillus. Accessed 28 October 2011

  • Vaughn T, Cavato T, Brar G, Coombe T, DeGooyer T, Ford S, Groth M, Howe A, Johnson S, Kolacz K, Pilcher C, Purcell J, Romano C, English L, Pershing J (2005) A method of controlling corn rootworm feeding using a Bacillus thuringiensis protein expressed in transgenic maize. Crop Sci 45:931–938

    Article  CAS  Google Scholar 

  • Vojtech E, Meissle M, Poppy GM (2005) Effects of Bt maize on the herbivore Spodoptera littoralis (Lepidoptera: Noctuidae) and the parasitoid Cotesia marginiventris (Hymenoptera: Braconidae). Transgenic Res 14:133–144

    Article  PubMed  CAS  Google Scholar 

  • Wilson MC, Shade RE (1966) Survival and development of larvae of the cereal leaf beetle, Oulema melanopus (Coleoptera: Chrysomelidae), on various species of Gramineae. Ann Entomol Soc Am 59:170–173

    Google Scholar 

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Acknowledgments

We are grateful to Franz Bigler and Fernando Álvarez-Alfageme for their valuable comments on an earlier draft of the manuscript and to Monsanto Company for providing maize seeds for the Bt and near-isogenic varieties.

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Correspondence to Michael Meissle.

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Meissle, M., Knecht, S., Waldburger, M. et al. Sensitivity of the cereal leaf beetle Oulema melanopus (Coleoptera: Chrysomelidae) to Bt maize-expressed Cry3Bb1 and Cry1Ab. Arthropod-Plant Interactions 6, 203–211 (2012). https://doi.org/10.1007/s11829-011-9178-8

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