Environmental risk assessment for the small tortoiseshell Aglais urticae and a stacked Bt‐maize with combined resistances against Lepidoptera and Chrysomelidae in central European agrarian landscapes
Abstract
The cultivation of Lepidoptera-resistant Bt-maize may affect nontarget butterflies. We assessed the risk posed by event MON89034 × MON88017 (expressing Cry1A.105 and Cry2Ab2 against corn borers) to nontarget Lepidoptera. Using the small tortoiseshell Aglais urticae, a butterfly species common in central Europe, as a test organism we (i) assessed the toxicity of Bt-maize pollen on butterfly larvae; (ii) measured pollen deposition on leaves of the host plant Urtica dioica; (iii) mapped the occurrence and distribution of host plants and larvae in two arable landscapes in Germany during maize anthesis; and (iv) described the temporal occurrence of a 1-year population of A. urticae. (i) Larvae-fed 200 Bt-maize pollen grains/cm(2) had a reduced feeding activity. Significant differences in developmental time existed at pollen densities of 300 Bt-maize pollen grains/cm(2) and in survival at 400 grains/cm(2). (ii) The highest pollen amount found was 212 grains/cm(2) at the field margin. Mean densities were much lower. (iii) In one region, over 50% of A. urticae nests were located within 5 m of a maize field, while in the other, all nests were found in more than 25 m distance to a maize field. (iv) The percentage of larvae developing during maize anthesis was 19% in the study area. The amount of pollen from maize MON89034 × MON88017 found on host plants is unlikely to adversely affect a significant proportion of larvae of A. urticae. This paper concludes that the risk of event MON89034 × MON88017 to populations of this species is negligible.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
During pollen shed, butterfly larvae are likely to ingest certain amounts of pollen grains together with their food plant.
“During the period of pollen shed, butterfly larvae are likely to ingest certain amounts of pollen grains together with their food plant (Perry et al., 2010;Schuppener et al., 2012;Shelton and Sears, 2001).”
From Genetically engineered crops help support conservation biological control (2019) · cites this paper as Schuppener et al., 2012
Cites
Bacillus thuringiensis and Its Pesticidal Crystal Proteins
Schnepf, E., Crickmore, N., Rie, J. V., Lereclus, D., Baum, J. A., Feitelson, J. S., Zeigler, D. R., & Dean, D. H. (1998) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.62.3.775-806.1998 · Cited by 3,062 · see citing works
Global Status of Commercialized biotech/GM crops
James, C. L. R. (2006) · Cited by 1,708 · see citing works
Transgenic pollen harms monarch larvae
Losey, J. E., Rayor, L. S., & Carter, M. E. (1999) · Nature · doi:10.1038/20338 · Cited by 1,182 · see citing works
Revision of the Nomenclature for the Bacillus thuringiensis Pesticidal Crystal Proteins
Crickmore, N., Zeigler, D. R., Feitelson, J. S., Schnepf, E., Rie, J. V., Lereclus, D., Baum, J. A., & Dean, D. H. (1998) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.62.3.807-813.1998 · Cited by 1,117 · see citing works
Areawide Suppression of European Corn Borer with Bt Maize Reaps Savings to Non-Bt Maize Growers
Hutchison, W. D., Burkness, E. C., Mitchell, P. D., Moon, R. D., Leslie, T. W., Fleischer, S. J., Abrahamson, M., Hamilton, K. L., Steffey, K. L., Gray, M. E., et al. (2010) · Science · doi:10.1126/science.1190242 · Cited by 759 · see citing works
Growth stages of mono- and dicotyledonous plants: BBCH Monograph
Meier, U. (2018) · Federal Research Centre for Cultivated Plants (Julius Kühn-Institut) · doi:10.5073/20180906-074619 · Cited by 716 · see citing works
Growth stages of mono- and dicotyledonous plants
Meier, U. (1997) · Cited by 576 · see citing works
Insecticidal activity of Bacillus thuringiensis crystal proteins
van Frankenhuyzen, K. (2009) · Journal of Invertebrate Pathology · doi:10.1016/j.jip.2009.02.009 · Cited by 511 · see citing works
Impact of Bt corn pollen on monarch butterfly populations: A risk assessment
Sears, M. K., Hellmich, R. L., Stanley-Horn, D. E., Oberhauser, K. S., Pleasants, J. M., Mattila, H. R., Siegfried, B. D., & Dively, G. P. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.211329998 · Cited by 492 · see citing works
Guidance on the environmental risk assessment of genetically modified plants
(GMO), E. P. O. G. M. O. (2010) · EFSA Journal · doi:10.2903/j.efsa.2010.1879 · Cited by 428 · see citing works
Monarch larvae sensitivity to Bacillus thuringiensis - purified proteins and pollen
Hellmich, R. L., Siegfried, B. D., Sears, M. K., Stanley-Horn, D. E., Daniels, M. J., Mattila, H. R., Spencer, T., Bidne, K. G., & Lewis, L. C. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.211297698 · Cited by 273 · see citing works
Field deposition of Bt transgenic corn pollen: lethal effects on the monarch butterfly
Jesse, L. C. H., & Obrycki, J. J. (2000) · Oecologia · doi:10.1007/s004420000502 · Cited by 244 · see citing works
Temporal and spatial overlap between monarch larvae and corn pollen
Oberhauser, K. S., Prysby, M., Mattila, H. R., Stanley-Horn, D. E., Sears, M. K., Dively, G. P., Olson, E. R., Pleasants, J. M., Lam, W.-K. F., & Hellmich, R. L. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.211234298 · Cited by 234 · see citing works
Corn pollen deposition on milkweeds in and near cornfields
Pleasants, J. M., Hellmich, R. L., Dively, G. P., Sears, M. K., Stanley-Horn, D. E., Mattila, H. R., Foster, J. E., Clark, P., & Jones, G. D. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.211287498 · Cited by 224 · see citing works
Assessing the impact of Cry1Ab-expressing corn pollen on monarch butterfly larvae in field studies
Stanley-Horn, D. E., Dively, G. P., Hellmich, R. L., Mattila, H. R., Sears, M. K., Rose, R., Jesse, L. C. H., Losey, J. E., Obrycki, J. J., & Lewis, L. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.211277798 · Cited by 196 · see citing works
Dispersion and Deposition of Corn Pollen from Experimental Sources1
Raynor, G. S., Ogden, E. C., & Hayes, J. V. (1972) · Agronomy Journal · doi:10.2134/agronj1972.00021962006400040004x · Cited by 195 · see citing works
Absence of toxicity of Bacillus thuringiensis pollen to black swallowtails under field conditions
Wraight, C. L., Zangerl, A. R., Carroll, M. J., & Berenbaum, M. R. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.130202097 · Cited by 185 · see citing works
Nguyen, H. T., & Jehle, J. A. (2007) · Journal of Plant Diseases and Protection · doi:10.1007/bf03356208 · Cited by 170 · see citing works
Zangerl, A. R., McKenna, D. D., Wraight, C. L., Carroll, M. J., Ficarello, P., Warner, R., & Berenbaum, M. R. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.171315698 · Cited by 164 · see citing works
An aerobiological framework for assessing cross-pollination in maize
Aylor, D. E., Schultes, N. P., & Shields, E. J. (2003) · Agricultural and Forest Meteorology · doi:10.1016/s0168-1923(03)00159-x · Cited by 152 · see citing works
Dively, G. P., Rose, R., Sears, M. K., Hellmich, R. L., Stanley-Horn, D. E., Calvin, D. D., Russo, J. M., & Anderson, P. L. (2004) · Environmental Entomology · doi:10.1603/0046-225x-33.4.1116 · Cited by 137 · see citing works
Field measurements of airborne concentration and deposition rate of maize pollen
Jarosz, N., Loubet, B., Durand, B., et al. (2003) · Agricultural and Forest Meteorology · doi:10.1016/s0168-1923(03)00118-7 · Cited by 135 · see citing works
Extrapolating non-target risk of <i>Bt</i> crops from laboratory to field
Duan, J. J., Lundgren, J. G., Naranjo, S., & Marvier, M. (2010) · Biology Letters · doi:10.1098/rsbl.2009.0612 · Cited by 127 · see citing works
Modelling butterfly distribution based on remote sensing data
Luoto, M., Kuussaari, M., & Toivonen, T. (2002) · Journal of Biogeography · doi:10.1046/j.1365-2699.2002.00728.x · Cited by 97 · see citing works
Lee, M. K., Curtiss, A., Alcantara, E. P., et al. (1996) · Applied and Environmental Microbiology · doi:10.1128/aem.62.2.583-586.1996 · Cited by 96 · see citing works
Perry, J. N., Devos, Y., Arpaia, S., Bartsch, D., Gathmann, A., Hails, R. S., Kiss, J., Lheureux, K., Manachini, B., Mestdagh, S., et al. (2010) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2009.2091 · Cited by 91 · see citing works
DIURNAL PATTERNS OF POLLEN EMISSION IN AMBROSIA, PHLEUM, ZEA, AND RICINUS
Ogden, E. C., Hayes, J. V., & Raynor, A. G. S. (1969) · American Journal of Botany · doi:10.1002/j.1537-2197.1969.tb07500.x · Cited by 84 · see citing works
A Possible Infection Pathway in the Development of a Nuclear Polyhedrosis Virus
Harrap, K. A., & Robertson, J. S. (1968) · Journal of General Virology · doi:10.1099/0022-1317-3-2-221 · Cited by 79 · see citing works
Expression of Cry3Bb1 in transgenic corn MON88017
Nguyen, H. T., & Jehle, J. A. (2009) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf901115m · Cited by 78 · see citing works
Wolt, J. D., Peterson, R. K. D., Bystrak, P. G., et al. (2003) · Environmental Entomology · doi:10.1603/0046-225x-32.2.237 · Cited by 76 · see citing works
Lang, A., & Otto, M. (2010) · Entomologia Experimentalis et Applicata · doi:10.1111/j.1570-7458.2010.00981.x · Cited by 73 · see citing works
Eulerian modelling of pollen dispersal over heterogeneous vegetation canopies
Dupont, S., Brunet, Y., & Jarosz, N. (2006) · Agricultural and Forest Meteorology · doi:10.1016/j.agrformet.2006.09.004 · Cited by 72 · see citing works
Lang, A., & Vojtech, E. (2005) · Basic and Applied Ecology · doi:10.1016/j.baae.2005.10.003 · Cited by 68 · see citing works
Wu, X., Leonard, B. R., Zhu, Y. C., Abel, C. A., Head, G., & Huang, F. (2008) · Journal of Invertebrate Pathology · doi:10.1016/j.jip.2008.10.003 · Cited by 62 · see citing works
PERRY, J. N., Devos, Y., Arpaia, S., Bartsch, D. K., Ehlert, C., Gathmann, A., Hails, R. S., Hendriksen, N. B., Kiss, J. G., Messéan, A., et al. (2011) · Journal of Applied Ecology · doi:10.1111/j.1365-2664.2011.02083.x · Cited by 61 · see citing works
Laboratory studies on the effects of pollen from Bt‐maize on larvae of some butterfly species
Felke, M., Lorenz, N., & Langenbruch, G. A. (2002) · Journal of Applied Entomology · doi:10.1046/j.1439-0418.2002.00668.x · Cited by 54 · see citing works
Ventilation Required to Entrain Small Particles from Leaves
Aylor, D. E., & Parlange, J. ‐. (1975) · PLANT PHYSIOLOGY · doi:10.1104/pp.56.1.97 · Cited by 50 · see citing works
Ibargutxi, M. A., Muñoz, D., de Escudero, Í. R., et al. (2008) · Biological Control · doi:10.1016/j.biocontrol.2008.07.003 · Cited by 48 · see citing works
Effects of Cry1Ab-Expressing Corn Anthers on Monarch Butterfly Larvae
Anderson, P. L., Hellmich, R. L., Sears, M. K., Sumerford, D. V., & Lewis, L. C. (2004) · Environmental Entomology · doi:10.1603/0046-225x-33.4.1109 · Cited by 48 · see citing works
Schmitz, G., Bartsch, D. K., & Pretscher, P. (2003) · Environmental Biosafety Research · doi:10.1051/ebr:2003007 · Cited by 47 · see citing works
van Hout, R., Chamecki, M., Brush, G. S., et al. (2008) · Agricultural and Forest Meteorology · doi:10.1016/j.agrformet.2008.02.009 · Cited by 41 · see citing works
Aviron, S., Sanvido, O., Romeis, J., Herzog, F., & Bigler, F. (2009) · Agriculture Ecosystems & Environment · doi:10.1016/j.agee.2009.01.007 · Cited by 38 · see citing works
Hofmann, F., Epp, R., Kruse, L., Kalchschmied, A., Maisch, B., Müller, E., Kühn, U., Kratz, W., Ober, S., Radtke, J., et al. (2010) · Environmental Sciences Europe · doi:10.1007/s12302-010-0133-6 · Cited by 34 · see citing works
Drought reduces breeding success of the butterfly Aglais urticae
POLLARD, E., Greatorex-Davies, J. N., & Thomas, J. A. (1997) · Ecological Entomology · doi:10.1046/j.1365-2311.1997.00064.x · Cited by 34 · see citing works
Felke, M., Langenbruch, G. A., Feiertag, S., & Kassa, A. (2010) · Environmental Biosafety Research · doi:10.1051/ebr/2010006 · Cited by 32 · see citing works
Lessons we can learn from ecological biosafety research
Bartsch, D. K., & Schuphan, I. (2002) · Journal of Biotechnology · doi:10.1016/s0168-1656(02)00087-1 · Cited by 29 · see citing works
Response of Danaus plexippus to pollen of two new Bt corn events via laboratory bioassay
Mattila, H. R., Sears, M. K., & Duan, J. J. (2005) · Entomologia Experimentalis et Applicata · doi:10.1111/j.1570-7458.2005.00304.x · Cited by 28 · see citing works
Saarinen, K. (2002) · Agriculture Ecosystems & Environment · doi:10.1016/s0167-8809(01)00168-2 · Cited by 26 · see citing works
Auswirkungen des Pollens von transgenem Bt-Mais auf ausgewählte Schmetterlingslarven
Felke, M., & Langenbruch, G. A. (2005) · Cited by 19 · see citing works
Li, W., Wu, K., Wang, X.-Q., Wang, G., & Guo, Y. (2005) · Environmental Entomology · doi:10.1603/0046-225x-34.4.922 · Cited by 18 · see citing works
The airborne pollen flow of maize (Zea mays L.) in a multi-crop designed field plot
Vogler, A., Wettstein-Bättig, M., Aulinger‐Leipner, I., et al. (2009) · Agricultural and Forest Meteorology · doi:10.1016/j.agrformet.2009.05.008 · Cited by 13 · see citing works
Increased mortality of isolated first instar larvae ofInachis io(Lepidoptera)
Lauber, É., & Darvas, B. (2009) · Acta Phytopathologica et Entomologica Hungarica · doi:10.1556/aphyt.44.2009.1.11 · Cited by 8 · see citing works
German GM research—a personal account
Rauschen, S. (2009) · Nature Biotechnology · doi:10.1038/nbt0409-318 · Cited by 8 · see citing works
Self-citationMonitoring or Surveillance? Balancing between theoretical frameworks and practical experiences
Sanvido, O., Romeis, J., & Bigler, F. (2009) · Journal of Consumer Protection and Food Safety · doi:10.1007/s00003-009-0354-z · Cited by 8 · see citing works
Introgression of GM plants and the EU guidance note for monitoring.
den Nijs, H. C. M., & Bartsch, D. K. (2004) · CABI Publishing eBooks · doi:10.1079/9780851998169.0365 · Cited by 7 · see citing works
The population crash of the Small Tortoiseshell Aglais urticae
Jones, S. K. (2003) · The entomologist s record and journal of variation · Cited by 1 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Genetically engineered crops help support conservation biological control
Romeis, J., Naranjo, S. E., Meissle, M., & Shelton, A. M. (2019) · Biological Control · doi:10.1016/j.biocontrol.2018.10.001 · Cited by 231 · see citing works
“period of pollen shed, butterfly larvae are likely to ingest certain amounts of pollen grains together with their food plant (Perry et al., 2010; Schuppener et al., 2012; Shelton and Sears, 2001).”
BackgroundSzénási, Á., Pálinkás, Z., Zalai, M., Schmitz, O. J., & Balog, A. (2014) · Scientific Reports · doi:10.1038/srep05315 · Cited by 39 · see citing works
Corrales Madrid, J. L., Martínez Carrillo, J. L., Osuna Martínez, M. B., Durán Pompa, H. A., Alonso Escobedo, J., Javier Quiñones, F., Garzón Tiznado, J. A., Castro Espinoza, L., Zavala García, F., Espinoza Banda, A., et al. (2018) · Journal of Applied Entomology · doi:10.1111/jen.12499 · Cited by 17 · see citing works
- Authors
- SCHUPPENER, M., MÜHLHAUSE, J., MÜLLER, A., & RAUSCHEN, S.
- Affiliations
- RWTH Aachen University (DE)
- University of Göttingen (DE)
- Corresponding author
- SCHUPPENER, MECHTHILD
- ORCID
- RAUSCHEN, STEFAN
- Venue
- Molecular Ecology
- Publisher
- Wiley
- Published
- 2012-07-31
- Volume
- 21
- Issue
- 18
- Pages
- 4646-4662
- ISSN
- 0962-1083 (ISSN-L)
- 1365-294X
- OpenAlex
- W2151426328
- Cited by
- 37
- References
- 56
- Citations by year
- 2025: 1 · 2024: 1 · 2022: 2 · 2021: 3 · 2020: 3 · 2019: 5 · 2018: 5 · 2017: 5 · 2016: 2 · 2015: 4 · 2014: 4 · 2013: 2
- FWCI
- 3.65
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- Locations
- Molecular Ecology (publishedVersion)
- PubMed (publishedVersion)
- GRO (submittedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Genetically Modified Organisms Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Insect Resistance and Genetics
- Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect-Plant Interactions and Control
- Keywords
- small tortoiseshell, Bt maize, Cry1A.105, Cry2Ab2, Urtica dioica, larval survival, arable landscape, Central Europe, environmental risk assessment
- MeSH terms
- Bacillus thuringiensis Toxins, Animals, Bacillus thuringiensis, Bacterial Proteins, Butterflies, Zea mays, Endotoxins, Germany, Hemolysin Proteins, Larva, Pollen, Risk Assessment, Plants, Genetically Modified, Herbivory
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
