Increased mortality is predicted of Inachis io larvae caused by Bt-maize pollen in European farmland

Ecological Modelling

Volumn 250, Issue , 2013, Pages 126-133

  Holst, Niels ^a   Lang, Andreas ^b   Lövei, Gabor ^a   Otto, Mathias ^c  

^a AARHUS UNIVERSITY   (Denmark)

^b UNIVERSITY OF BASEL   (Switzerland)

^c Federal Agency for Nature Conservation   (Germany)

Author keywords

Bt maize; Dose response; GMO; Lepidoptera; Risk; Simulation model

Indexed keywords

BT-MAIZE; DOSE RESPONSE; GMO; LEPIDOPTERA; SIMULATION MODEL;

COMPUTER SIMULATION; COMPUTER SOFTWARE REUSABILITY; CULTIVATION; GRAIN (AGRICULTURAL PRODUCT); PHENOLS; RISKS;

PLANTS (BOTANY);

AGRICULTURAL LAND; BUTTERFLY; CULTIVATION; DOSE-RESPONSE RELATIONSHIP; ECOLOGICAL MODELING; ENVIRONMENTAL RISK; FOOD ORGANISM; GENETICALLY MODIFIED ORGANISM; HERB; HERBIVORE; LARVA; MAIZE; MORTALITY; PHENOLOGY; POLLEN; SOFTWARE;

EUROPE;

HEXAPODA; INACHIS IO; LEPIDOPTERA; PAPILIONOIDEA; URTICA DIOICA; ZEA MAYS;

EID: 84870912880     PISSN: 03043800     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ecolmodel.2012.11.006     Document Type: Article

References (67)

1. Abkin, M.H., Wolf, C., 1976. Distributed Delay Routines. Class Document No. 8. Dept Agric Econom, Michigan State Univ., East Lansing, USA.
2. Andow D.A., Lövei G.L., Arpaia S. Bt transgenic crops, natural enemies and implications for environmental risk assessment. Nature Biotechnology 2006, 24:749-751.
3. Arpaia S. Genetically modified plants and non-target organisms: analysing the functioning of the agro-ecosystem. Collection of Biosafety Reviews (ICGEB Biosafety Unit) 2010, 5:12-80.
4. Aylor D.N., Schultes N.P., Shields E.J. An aerobiological framework for assessing cross-pollination in maize. Agricultural and Forest Meteorology 2003, 119:111-129.
5. Bryant S.R., Thomas C.D., Bale J.S. Thermal ecology of gregarious and solitary nettle-feeding nymphalid butterfly larvae. Oecologia (Berlin) 2000, 122:1-10.
6. Bryant S.R., Thomas C.D., Bale J.S. The influence of thermal ecology on the distribution of three nymphalid butterflies. Journal of Applied Ecology 2002, 39:43-55.
7. Catacora-Vargas, G., 2011. Genetically modified organisms. A summary of potential adverse effects relevant to sustainable development. Biosafety Report 2011/12. GenØk Centre for Biosafety, Tromsø, Norway.
8. CERA, 2010. GM Crop Database. Center for Environmental Risk Assessment (CERA), Washington, DC, http://www.cera-gmc.org/index.php?action=gm_crop_database.
9. Dively G.P., Rose R., Sears M.K., Hellmich R.L., Stanley-Horn D.E., Calvin D.D., et al. Effects on monarch butterfly larvae (Lepidoptera: Danaidae) after continuous exposure to Cry1Ab-expressing corn during anthesis. Environmental Entomology 2004, 33:1116-1125.
10. Ebert G., Rennwald E. Die Schmetterlinge Baden-Württembergs, Band 1: Tagfalter I 1991, Verlag Eugen Ulmer, Stuttgart, Germany.
11. Felke M., Langenbruch G.A. Effect of Bt-maize-pollen on caterpillars of Inachis io in a laboratory assay. Gesunde Pflanz 2003, 55:1-7.
12. Felke M., Langenbruch G.A. Impact of transgenic Bt-maize pollen on larvae of selected butterflies. BfN-Skripten 157 2005, Bundesamt für Naturschutz, Bonn, Germany.
13. Felke M., Langenbruch G.A., Feiertag S., Kassa A. Effect of Bt-176 maize pollen on first instar larvae of the Peacock butterfly (Inachis io) (Lepidoptera; Nymphalidae). Environmental Biosafety Research 2010, 9:5-12.
14. van Frankenhuyzen K. Insecticidal activity of Bacillus thuringiensis crystal proteins. Journal of Invertebrate Pathology 2009, 101:1-16.
15. Gao Y., Oppert B., Lord J.C., Liu C., Lei Z. Bacillus thuringiensis Cry3Aa toxin increases the susceptibility of Crioceris quatuordecimpunctata to Beauveria bassiana infection. Journal of Invertebrate Pathology 2012, 109:260-263.
16. Gutierrez A.P. Applied Population Ecology 1996, John Wiley & Sons, New York.
17. Gutierrez A.P., Neuenschwander P., Schulthess F., Herren H.R., Baumgaertner J.U., Wermelinger B., et al. Analysis of biological control of cassava pests in Africa. II. Cassave mealybug Phenacoccus manihoti. Journal of Applied Ecology 1988, 25:921-940.
18. Hansen Jesse L.C., Obrycki J.J. Field deposition of Bt transgenic corn pollen: lethal effects on the monarch butterfly. Oecologia (Berlin) 2000, 125:241-248.
19. Hofmann F., Epp R., Kalchschmid A., Kratz W., Kruse L., Kuhn U., et al. Monitoring of Bt-maize pollen exposure in the vicinity of the nature reserve Ruhlsdorfer Bruch in northeast Germany 2007 to 2008. Umweltwiss Schadst-Forsch 2010, 22:229-251.
20. Hofmann F., Jannicke L., Jannicke U., Wachter R., Kuhn U. Modellrechnungen zur Ausbreitung von Maispollen unter Worst-Case-Annahmen mit Vergleich von Freilandmessdaten 2008, ökologie Büro, Bremen, Germany.
21. Hofmann F., Otto M., Kuhn U., Ober S., Schlechtriemen U., Vögel R. A new method for in situ measurement of Bt-maize pollen deposition on host-plant leaves. Insects 2011, 2:12-21.
22. Holst N. A universal simulator for ecological models. Ecological Informatics 2012, http://dx.doi.org/10.1016/j.ecoinf.2012.11.001, in press.
23. James C. Global Status of Commercialized Biotech/GM Crops 2011 2011, ISAAA, Ithaca, NY.
24. Kawashima S., Matsuo K., Du M., Takahashi Y., Inoue S., Yonemura S. An algorithm for estimating potential deposition of corn pollen for environmental assessment. Environmental Biosafety Research 2004, 3:197-207.
25. Kolligs D. Schmetterlinge Schleswig-Holsteins 2003, Wachholtz Verlag, Neumünster, Germany.
26. Koziel M.G., Beland G.L., Bowman C., Carozzi N.B., Crenshaw R., Crossland L., et al. Field performance of elite transgenic maize plants expressing an insecticidal protein derived from Bacillus thuringiensis. BioTechnology 1993, 11:194-200.
27. Lang A., Brunzel S., Dolek M., Otto M., Theissen B., Lauber E., et al. Modelling in the light of uncertainty of key parameters: a call to exercise caution in field predictions of Bt-maize effects. Proceedings of the Royal Society of London Series B: Biological Sciences 2011, 278:980-981.
28. Lang A., Ludy C., Vojtech E. Dispersion and deposition of Bt maize pollen in field margins. Journal of Plant Diseases and Protection 2004, 111:417-428.
29. Lang A., Otto M. A synthesis of laboratory and field studies on the effects of transgenic Bacillus thuringiensis (Bt) maize on non-target Lepidoptera. Entomologia Experimentalis et Applicata 2010, 135:121-134.
30. Lang A., Vojtech E. The effects of pollen consumption of transgenic Bt maize on the common swallowtail, Papilio machaon L. (Lepidoptera, Papilionidae). Basic and Applied Ecology 2006, 7:296-306.
31. Lauber, E., 2011. Cry1 toxin content of MON 810 Bt-corn and the effect of its pollen on protected butterfly species in Hungary, PhD Thesis. University of Budapest, Hungary.
32. Lauber E., Darvas B. Increased mortality of isolated first instar larvae of Inachis io (Lepidoptera). Acta Phytopathologica et Entomologica Hungarica 2009, 44:111-117.
33. Losey J.E., Hutbauer R.E., Hartzler R.G. Enumerating lepidopteran species associated with maize as a first step in risk assessment in the USA. Environmental Biosafety Research 2003, 2:247-261.
34. Losey J.E., Rayor L.S., Carter M.E. Transgenic pollen harms monarch larvae. Nature 1999, 399:214.
35. Lövei G.L. Ecological risks and benefits of transgenic plants. New Zealand Plant Protection 2001, 54:93-100.
36. Mahmoud A.M.A., Luna-Santillana E.J., Rodríguez-Perez M.A. Parasitism by the endoparasitoid, Cotesia flavipes induces cellular immunosuppression and enhances susceptibility of the sugar cane borer, Diatraea saccharalis to Bacillus thuringiensis. Journal of Insect Science (Madison) 2011, 11:119.
37. Manetsch T.J. Time-varying distributed delays and their use in aggregate models of large systems. IEEE Transactions on Systems, Man, and Cybernetics 1976, SMC-6:547-553.
38. Martin R.C. Agile Software Development: Principles, Patterns, and Practices 2006, Prentice-Hall, Upper Saddle River, NJ.
39. Miller W.E. Reproductive bulk in capital-breeding Lepidoptera. The Journal of the Lepidopterists' Society 2005, 59:229-233.
40. Nguyen, H.T., 2004. Sicherheitsforschung und Monitoringmethoden zum Anbau von Bt-Mais: Expression, Nachweis und Wirkung von rekombinantem Cry1Ab in heterologen Expressionssystemen, PhD Thesis. Georg-August-Universität Göttingen, Germany.
41. Nguyen H.T., Jehle J.A. Quantitative analysis of the seasonal and tissue-specific expression of Cry1Ab in transgenic maize Mon810. Journal of Plant Diseases and Protection 2007, 114:82-87.
42. Ohlfest J.R., Jesse L.C., Jurenka R., Obrycki J.J. Stability of insecticidal CryIAb protein in transgenic Bt corn pollen exposed to UV radiation. Journal of the Kansas Entomological Society 2002, 75:48-51.
43. Olofsson M., Vallin A., Jakobsson S., Wiklund C. Winter predation on two species of hibernating butterflies: monitoring rodent attacks with infrared cameras. Animal Behaviour 2011, 81:529-534.
44. Peacock J.W., Schweitzer D.F., Carter J.L., Dubois N.R. Laboratory assessments of the effects of Bacillus thuringiensis on native Lepidoptera. Environmental Entomology 1998, 27:450-457.
45. Perry J.N., Devos Y., Arpaia S., Bartsch D., Ehlert C., Gathmann A., et al. Estimating the effects of Cry1F Bt-maize pollen on non-target Lepidoptera using a mathematical model of exposure. Journal of Applied Ecology 2012, 49:29-37.
46. Perry J.N., Devos Y., Arpaia S., Bartsch D., Gathmann A., Hails R.S., et al. A mathematical model of exposure of nontarget Lepidoptera to Bt-maize pollen expressing Cry1Ab within Europe. Proceedings of the Royal Society of London Series B: Biological Sciences 2010, 277:1417-1425.
47. Perry J.N., Devos Y., Arpaia S., Bartsch D., Gathmann A., Hails R.S., et al. The usefulness of a mathematical model of exposure for environmental risk assessment. Proceedings of the Royal Society of London Series B: Biological Sciences 2011, 278:982-984.
48. Peterson R.K.D., Meyer S.J., Wolf A.T., Wolt J.D., Davis P.M. Genetically engineered plants, endangered species, and risk: a temporal and spatial exposure assessment for Karner Blue Butterfly larvae and Bt maize pollen. Risk Analysis 2006, 26:845-858.
49. Pleasants J.M., Hellmich R.L., Dively G.P., Sears M.K., Stanley-Horn D.E., Mattila H.R., et al. Corn pollen deposition on milkweeds in and near cornfields. Proceedings of the National Academy of Science 2001, 98:11919-11924.
50. Pullin A.S. Changes in leaf quality following clipping and regrowth of Urtica dioica, and consequences for a specialist insect herbivore, Aglais urticae. Oikos 1987, 49:39-45.
51. R Development Core Team R: A Language and Environment for Statistical Computing 2011, R Foundation for Statistical Computing, Vienna, Austria.
52. Ritz C., Streibig J.C. Bioassay analysis using R. Journal of Statistical Software 2005, 12(5).
53. Schmitz G., Bartsch D., Pretscher P. Selection of relevant non-target herbivores for monitoring the environmental effects of Bt maize pollen. Environmental Biosafety Research 2003, 2:117-132.
54. Schulte, T., Eller, O., Niehuis, M., Rennewlad, E., 2007. Die Tagfalter der Pfalz, Band 1. Fauna und Flora in Rheinland-Pfalz, Beiheft 36. Gesellschaft für Naturschutz und Ornithologie Rheinland-Pfalz, Landau, Germany.
55. Sears M.K., Hellmich R.L., Stanley-Horn D.E., Oberhauser K.S., Pleasants J.M., Mattila H.R., et al. Impact of Bt corn pollen on monarch butterfly populations: a risk assessment. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:11937-11942.
56. Shirai Y., Takahashi M. Effects of transgenic Bt corn pollen on a non-target lycaenid butterfly, Pseucozizeeria maha. Applied Entomology and Zoology 2005, 40:151-159.
57. Silvert W. Object-oriented ecosystem modeling. Ecological Modelling 1993, 68:91-118.
58. Szekacs A., Lauber E., Juracsek J., Darvas B. Cry1Ab toxin production of MON810 transgenic maize. Environmental Toxicology and Chemistry 2010, 29:182-190.
59. Traxler, A., Minarz, E., Höttinger, H., Pennerstorfer, J., Schmatzberger, A., Banko, G. et al. 2005. Biodiversitäts-Hotspots der Agrarlandschaft als Eckpfeiler für Risikoabschätzung und Monitoring von GVO. Bundesministerium für Gesundheit und Frauen, Forschungsberichte der Sektion IV, Wien, Austria.
60. USDA, 2011. Biotechnology varieties. Acreage 2011; June 2011: 25. USDA National Agricultural Statistics Service, Washington, DC.
61. Van Rie J. Bacillus thuringiensis and its use in transgenic insect control technologies. International Journal of Medical Microbiology 2000, 290:463-469.
62. Vansickle J. Attrition in distributed delay models. IEEE Transactions on Systems, Man, and Cybernetics 1977, 7:635-638.
63. Velky M., Kanuch P., Kristin A. Food composition of wintering great tits (Parus major): habitat and seasonal aspects. Folia Zoologica 2011, 60:228-236.
64. Westgate M.E., Lizaso J., Batchelor W. Quantitative relationships between pollen shed density and grain yield in maize. Crop Science 2003, 43:934-942.
65. Wiklund C., Gotthard K., Nylin S. Mating system and the evolution of sex-specific mortality rates in two nymphalid butterflies. Proceedings of the Royal Society of London Series B: Biological Sciences 2003, 270:1823-1828.
66. Wilson J. Population changes in three butterfly species in North Lancashire 1979 to 1990. Naturalist (Rotherham) 1991, 116:95-98.
67. Wolt J.D., Conlan C.A., Majima K. An ecological risk assessment of Cry1F maize pollen impact to pale grass blue butterfly. Environmental Biosafety Research 2005, 4:243-251.