A mathematical model of exposure of nontarget Lepidoptera to Bt-maize pollen expressing Cry1Ab within Europe

Proceedings of the Royal Society B: Biological Sciences

Volumn 277, Issue 1686, 2010, Pages 1417-1425

  Perry, J N ^a   Devos, Y ^b   Arpaia, S ^c   Bartsch, D ^d   Gathmann, A ^d   Hails, R S ^e   Kiss, J ^f   Lheureux, K ^b   Manachini, B ^g   Mestdagh, S ^b   Neemann, G ^h   Ortego, F ⁱ   Schiemann, J ^j   Sweet, J B ^k  

^a Oaklands Barn   (United Kingdom)

^b EUROPEAN FOOD SAFETY AUTHORITY   (Italy)

^c National Agency for New Technologies   (Italy)

^d Bundesamt fur Verbraucherschutz und Lebensmittelsicherheit   (Germany)

^e Centre for Ecobgy and Hydrobgy   (United Kingdom)

^f SZENT ISTVÁN UNIVERSITY   (Hungary)

^g UNIVERSITY OF PALERMO   (Italy)

^h Büro für Landschaftsökologie und Umweltstudien BLaU   (Germany)

ⁱ CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^j INSTITUTE FOR EPIDEMIOLOGY AND PATHOGEN DIAGNOSTICS   (Germany)

^k Sweet Environmental Consultants   (United Kingdom)

more..

Author keywords

Cry1ab; Exposure; Genetically modified maize; Mathematical model; Non target lepidoptera; Risk assessment

Indexed keywords

BUTTERFLY; DOSE-RESPONSE RELATIONSHIP; HOST PLANT; MAIZE; MORTALITY; MOTH; NUMERICAL MODEL; POLLEN; PROTEIN; RISK ASSESSMENT; TRANSGENIC PLANT;

EUROPE;

BACILLUS THURINGIENSIS; INACHIS; LEPIDOPTERA; OSTRINIA NUBILALIS; PAPILIONOIDEA; PLUTELLA XYLOSTELLA; VANESSA ATALANTA; ZEA MAYS;

EID: 77952254043     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2009.2091     Document Type: Article

References (51)

1. Anderson, P. L., Hellmich, R. L., Prasifka, J. R. & Lewis, L. C. 2005 Effects on fitness and behavior on monarch butterfly larvae exposed to a combination of Cry1Abexpressing corn anthers and pollen. Environ. Entomol. 34, 944-952. (doi:10.1603/0046-225X-34.4.944)
2. Annamalai,S.,Ito,Y.&Saito,T. 1988Populationfluctuationsofthediamondbackmoth,Plutellaxylostella(L.) oncabbagesinBacillusthuringiensissprayedandnonsprayedplotsandfactorsaffectingw ithin-generationsurvivalofimmatures.Res.PopulEcol.30,329-342.(doi:10.1007/ BF02513253)(Pubitemid20422102)
3. Aviron, S., Sanvido, O., Romeis, J., Herzog, F. & Bigler, F. 2009 Case-specific monitoring of butterflies to determine potential effects of transgenic .Bt-maize in Switzerland. Agrie. Ecosyst. Environ. 131, 137-144. (doi:10.1016/j. agee.2009.01.007)
4. BEETLE Report 2009 Long-term effects of genetically modified (GM) crops on health and the environment (including biodiversity): prioritization of potential risks and delimitation of uncertainties. BEETLE Final Report, German Federal Office of Consumer Protection and Food Safety, BLaU-Umweltstudien and Genius GmbH. See http://ec.europa.eu/environment/biotechnology/ pdf/beetle-report.pdf.
5. Conrad, K. F., Warren, M. S., Fox, R., Parsons, M. S. & Woiwod, I. P. 2006 Rapid declines of common, widespread British moths provide evidence of an insect biodiversity crisis. Biol. Conserv. 132, 279-291. (doi:10. 1016/j.biocon.2006.04.020) (Pubitemid 44015688)
6. Crickmore, N. 2005 Using worm to better understand how Bacillus thuringiensis kills insects. Trends Microbiol. 13, 347-350. (doi:10.1016/j.tim. 2005.06.002) (Pubitemid 41073803)
7. Darvas, B., Csóti, A., Adel, G., Peregovits, L., Ronkay, L., Lauber, É. & Polgár, L. 2004 Some data to the risk analysis of Bt-corn pollen and protected lepidopteran species in Hungary (in Hungarian). Növényvédelem 40, 441-449.
8. Devos, Y., Reheul, D. & De Schrijver, A. 2005 The coexistence between transgenic and nontransgenic maize in the European union: a focus on pollen flow and cross-fertilization. Environ. Biosafety Res. 4, 71-87. (doi:10.1051/ebr:2005013)
9. 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 Effects on monarch butterfly larvae (Lepidoptera: Danaidae) after continuous exposure to CrylAb-expressing corn during anthesis. Environ. Entomol 33, 1116-1125. (doi:10.1603/0046-225X-33. 4.1116)
10. Eastham, K. & Sweet, J. 2002 Genetically modified organisms (GMOs): The significance of gene flow through pollen transfer. European Environment Agency. See http://reports.eea.eu.int/environmental-issue-report-2002- 28/en/GMOs%20for%20www.pdf.
11. EFSA 2009 Scientific Opinion of the Panel on Genetically Modified Organisms on applications (EFSA-GMO-RXMON810) for the renewal of authorisation for the continued marketing of (1) existing food and food ingredients produced from genetically modified insect resistant maize MON810; (2) feed consisting of and/or containing maize MON810, including the use of seed for cultivation; and of (3) food and feed additives, and feed materials produced from maize MON810, all under Regulation (EC) No 1829/2003 from Monsanto. EFSA J. 1149, 1-85. See http://www.efsa.europa. eu/cs/BlobServer/Scientific-Opinion/gmo-op-ej1149- maizeMON810-finalopinion-en-rev.pdf.
12. Farinés, G. P., de la Poza, M., Hernández-Crespo, P., Ortego, F. & Castañera, P. 2004 Resistance monitoring of field populations of the corn borers Sesamia nonagrioides and Ostrinia nubilalù after 5 years of Bt-maize cultivation in Spain. Ent. Exp. Appl. 110, 23-30. (doi:10.1111/j.0013-8703.2004.00116.x)
13. Felke, M. & Langenbruch, A. 2005 Auswirkungen des Pollens von transgenem Bt-Mais auf ausgewählte Schmetterlingslarven. BfN-Skripten 157. See http://www.bfn.de/ fileadmin/MDB/documents/skript 157.pdf.
14. Felke, M., Lorenz, N. & Langenbruch, A. 2002 Laboratory studies on the effects of pollen from Bi-maize on larvae of some butterfly species. J. Appl. Entomol. 126, 320-325. (doi:10.1046/j.1439-0418.2002.00668.x)
15. Felke, M., Lorenz, N., Langenbruch, G.-A., Feiertag, S. & Kassa, A. In press. Effect of Bt-176 maize pollen on first instar larvae of the Peacock butterfly (Inachis io) (Lepidoptera; Nymphalidae). Environ. Biosafety Res.
16. Gathmann, A., Wirooks, L., Eckert, J. & Schuphan, I. 2006a Spatial distribution of Aglais urticae (L.) and its host plant Urtica dioica (L.) in an agricultural landscape: implications for Bt-maize risk assessment and post-market monitoring. Environ. Biosafety Res. 5, 27-36. (doi: 10. 1051/ebr:2006014) (Pubitemid 44574286)
17. Gathmann, A., Wirooks, L., Hothhorn, L. A., Bartsch, D. & Schuphan, I. 2006b Impact of Bt-maize pollen (MON810) on lepidopteran larvae living on accompanying weeds. Mol. Ecol. 15, 2677-2685. (doi:10.1111/j. 1365-294X.2006.02962.x) (Pubitemid 44050731)
18. Gómez-Barbero, M., Berbel, J. & Rodríguez-Cerezo, E. 2008 Adoption and performance of the first GM crop introduced in EU agriculture: Bt-maize in Spain. European Commission, Joint Research Centre, Institute for Prospective Technological Studies. See http://ftp.jrc.es/ EURdoc/JRC37046.pdf.
19. Griego, V. M. & Spence, K. D. 1978 Inactivation of Bacillus thuringiensis; spores by ultraviolet and visible light. Appl. Environ. Microbiol. 35, 906-910.
20. Hellmich, R. L., Siegfried, B., Sears, M. K., Stanley-Horn, D. E., Mattila, H. R., Spencer, T., Bidne, K. G. Lewis, L. C. 2001 Monarch larvae sensitivity to Bacillus thuringiensis purified proteins and pollen. Proc. Natl Acad. Sci. USA 98, 11925-11930. (doi:10.1073/pnas.211297698) (Pubitemid 32959803)
21. Hofmann, F. 2007 Kurzgutachten zur Abschätzung der Maispollendeposition in Relation zur Entfernung von Maispollenquellen mittels technischem Pollensammler PMF, Gutachten für das Bundesamt für Naturschutz BfN . See http://www.bfn.de/fileadmin/MDB/documents/ themen/agrogentechnik/07-05-31-Gutachten-Pollende position-end.pdf.
22. Hofmann, F. 2009 Modellrechnungen zur Ausbreitung von Maispollen unter worst-case-Annahmen mit vergleich zu Freilandmessungen, Gutachten für das Bundesamt für Naturschutz BfN. See http://www.bfh.de/fileadmin/ MDB/documents/service/Hofmann-et-al-2009-Maispoll en-WorstCase-Modell.pdf.
23. Jarosz, N., Loubet, B. & Huber, L. 2004 Modelling airborne concentration and deposition rate of maize pollen. Atmos. Environ. 38, 5555-5566. (doi:10.1016/j.atmosenv.2004. 06.027)
24. Jesse, L. C. H. & Obrycki, J. J. 2000 Field deposition of Bt transgenic corn pollen: lethal effects on the monarch butterfly. Oecobgia 125, 241-248.
25. Jesse, L. C. H. & Obrycki, J. J. 2003 Occurrence of Danaus plexippus L. (Lepidoptera: Danaidae) on milkweeds (Asclepias syriaca) in transgenic Bt corn agroecosystems. Agric. Ecosyst. Environ. 97, 225-233. (doi: 10.1016/ SO 167-8809 (03) 00124-5)
26. Lang, A. & Vojtech, E. 2006 The effects of pollen consumption on transgenic Bt-maize on the common swallowtail, Papilio machaon L. (Lepidoptera, Papilionidae). Basic Appl. Ecol. 7, 296-306. (doi:10.1016/j.baae.2005.10. 003)
27. Lang,A.,Ludy,C.Vojtech,E.2004DispersionanddepositionofBt- maizepolleninfieldmargins.Z.Pflanzenkr.Pflanzenschutz111,417-428. (Pubitemid39501133)
28. Liu, S. S., Wang, X. G., Guo, S. J., He, J. H. & Shi, Z. H. 2000 Seasonal abundance of the parasitoid complex associated with the diamondback moth, Plutella xybstella (Lepidoptera: Plutellidae) in Hangzhou, China. Bull. Entomol. Res. 90, 221-231.
29. Losey, J. E., Rayor, L. S. & Carter, M. E. 1999 Transgenic pollen harms monarch larvae. Nature 399, 214. (doi:10. 1038/20338)
30. Lozzia, G. C. & Manachini, B. 2003 Susceptibility of Ostrinia nubilalis to Bacillus thuringiensis var kurstaki. B. Insectol. 56, 215-219.
31. Mattila, H. R., Sears, M. K. & Duan, J. J. 2005 Response of Danaus plexippus to pollen of two new Bt corn events via laboratory bioassay. Entomol. Exp. Appl. 116, 31-41. (doi: 10.1111/j. 1570-7458.2005.00304.x)
32. Mendelsohn, M., Kough, J., Vaituzis, Z. & Matthews, K. 2003 Are Bt crops safe? Nat. Biotechnol. 21, 1003-1009. (doi:10.1038/nbt0903-1003) (Pubitemid 37064725)
33. Nguyen, H. T. & Jehle, J. A. 2007 Quantitative analysis of the seasonal and tissue-specific expression of Cry1Ab in transgenic maize MON810. Z. Pflanzenkr. Pflanzenschutz 114, 82-87.
34. Oberhauser, K. S. et al 2001 Temporal and spatial overlap between monarch larvae and corn pollen. Proc. Natl Acad. Sci USA 98, 11 913-11 918.
35. Obrist, L. B., Dutton, A., Albajes, R. & Bigler, F. 2006 Exposure of arthropod predators to Cry1Ab toxin in Btmaize fields. Ecol. Entomol 31, 143-154. (doi:10.1111/j. 0307-6946.2006.00762.x)
36. Peterson, R. K. D., Meyer, S. J., Wolf, A. T, Wolt, J. D. & Davis, P. M. 2006 Genetically engineered plants, endangered species, and risk: a temporal and spatial exposure assessment for Karner blue butterfly larvae and Btmaize pollen. Risk Anal. 26, 845-858. (doi:10.1111/j. 1539-6924.2006.00763.x)
37. Pleasants, J. M., Hellmich, R. L., Dively, G. P., Sears, M. K., Stanley-Horn, D. E., Mattila, H. R., Foster, J. E., Clark, T. L. & Jones, G. D. 2001 Corn pollen deposition on milkweeds in or near corn field. Proc. Natl Acad. Sci. USA 98, 11 919-11 924. (doi:10.1073/pnas.211287498)
38. Saeglitz, C., Engels, H. & Schuphan, I. 2006a Final Report of ProBenBt, Workpackage 1, Task 4. See http://www. bio5.rwth-aachen.de/german/ downloads/EU-Review.pdf.
39. Saeglitz, C., Bartsch, D., Eber, S., Gathmann, A., Priesnitz, K. U. & Schuphan, I. 2006b Monitoring the Cry1Ab susceptibility of European corn borer in Germany. J. Econ. Entomol. 99, 1768-1773. (doi:10.1603/0022-0493-99.5. 1768)
40. Schmitz, G., Pretscher, P. & Bartsch, D. 2003 Selection of relevant non-target herbivores for monitoring the environmental effects of Bt-maize pollen. Environ. Biosafety Res. 2, 117-132.
41. Scott, J. A. 1986 The butterflies of North America: a natural history and field guide. Stanford, CA: Stanford University Press.
42. Sears, M. K., Hellmich, R. L., Siegfried, B. D., Pleasants, J. M., Stanly-Horn, D. E., Oberhauser, K. S. & Dively, G. P. 2001 Impact of Bt corn pollen on monarch butterfly populations: a risk assessment. Proc. Natl Acad. Sci. USA 98, 11937-11942.
43. Soberón, M., Gill, S. S. & Bravo, A. 2009 Signaling versus punching hole: how do Bacillus thuringiensis toxins kill insect midgut cells? Cell. Mol Life Sci. 66, 1337-1359. (doi: 10.1007/s00018-008-8330-9)
44. Talekar, N. S. & Shelton, A. M. 1993 Biology, ecology, and management of the diamondback moth. Annu. Rev. Entomol 38, 275-301. (doi:10.1146/annurev. en.38.010193. 001423)
45. Traxler, A., Minarz, E., Höttinger, H., Pennerstorfer, J., Schmatzberger, A., Banko, G., Placer, K., Hadrbolec, M. & Gaugitsch, H. 2005 Biodiversitäts-hotspots der Agrarlandschaft als Eckpfeiler für Risikoabschätzung und Monitoring von GVO. Bundesministerium für Gesundheit und Frauen, Forschungsberichte der Sektion IV, Band 5/2005, Wien. See http://www.bio5.rwth-aachen. de/german/downloads/EU-Review.pdf.
46. Van Hout, R., Chamecki, M., Brush, G., Katz, J. & Parlange, M. B. 2008 The influence of local meteorological conditions on the circadian rhythm of corn (Zea mays L.) pollen emission. Agric. Forest Meteorol 148, 1078-1092.
47. Varley, G. C., Gradwell, G. R. & Hassell, M. P. 1973 Insect population ecology: an analytical approach. Oxford, UK: Blackwell.
48. Vogler, A., Wettstein-Bättig, M., Aulinger-Leipner, I. & Stamp, P. 2009 The airborne pollen flow of maize (Zea mays L.) in a multi-crop designed field plot. Agric. Forest Meteorol. 149, 1776-1780. (doi:10.1016/j.agrformet. 2009.05.008)
49. Wolt,J.D.,Peterson,R.K.D.,Bystrak,P.Maede,T. 2003Ascreeninglevelapproachfornontargetinsectriskassessment: transgenicBtcornpollenandthemonarchbutterfly(Lepidoptera:Danaidae).Environ. Entomol32,237-246.(doi:10.1603/0046-225X-32.2.237)(Pubitemid36516807)
50. Wolt, J. D., Conlan, C. A. Majima, K. 2005 An ecological risk assessment of Cry IF maize pollen impact to pale grass blue butterfly. Environ. Biosafety Res. 4, 243-251. (doi:10.1051/ebr:2006005) (Pubitemid 44155374)
51. Wraight, C. L., Zangerl, A. R., Carroll, M. J. & Berenbaum, M. R. 2000 Absence of toxicity of Bacillus thuringiensis pollen to black swallowtails under field conditions. Proc. Natl Acad. Sci. USA 97, 7700-7703. (doi:10.1073/pnas. 130202097)