Potential use of an arthropod database to support the non-target risk assessment and monitoring of transgenic plants

Transgenic Research

Volumn 23, Issue 6, 2014, Pages 995-1013

  Romeis, Jörg ^a   Meissle, Michael ^a   Álvarez Alfageme, Fernando ^a   Bigler, Franz ^a   Bohan, David A ^b   Devos, Yann ^c   Malone, Louise A ^d   Pons, Xavier ^e   Rauschen, Stefan ^f,g  

^a AGROSCOPE RECKENHOLZ TÄNIKON RESEARCH STATION ART   (Switzerland)

^b UNIV BOURGOGNE FRANCHE COMTÉ   (France)

^c EUROPEAN FOOD SAFETY AUTHORITY   (Italy)

^d THE NEW ZEALAND INSTITUTE FOR PLANT AND FOOD RESEARCH LIMITED   (New Zealand)

^e UNIVERSITY OF LLEIDA   (Spain)

^f RWTH AACHEN UNIVERSITY   (Germany)

^g FORSCHUNGSZENTRUM JÜLICH   (Germany)

Author keywords

Bt maize; Ecosystem services; Environmental risk assessment; Scenarios; Species selection; Transgenic maize

Indexed keywords

ARTHROPODA; ZEA MAYS;

ANIMAL; ARTHROPOD; BIOLOGICAL PEST CONTROL; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL MONITORING; FACTUAL DATABASE; MAIZE; PARASITOLOGY; PHYSIOLOGY; PREVENTION AND CONTROL; PROCEDURES; RISK ASSESSMENT; TOXICITY; TRANSGENIC PLANT;

ANIMALS; ARTHROPODS; DATABASES, FACTUAL; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL MONITORING; PEST CONTROL, BIOLOGICAL; PLANTS, GENETICALLY MODIFIED; RISK ASSESSMENT; ZEA MAYS;

EID: 84916941826     PISSN: 09628819     EISSN: 15739368     Source Type: Journal    
DOI: 10.1007/s11248-014-9791-2     Document Type: Article

References (96)

1. Abraham R, Kuroli G (2003) Role of mites and thrips in the agrobiocoenosis of the soybean. Commun Agric Appl Biol Sci 68:223–230
2. Agusti N, Bourguet D, Spataro T, Delos M, Eychenne N, Folcher L, Arditi R (2005) Detection, identification and geographical distribution of European corn borer larval parasitoids using molecular markers. Mol Ecol 14:3267–3274
3. Ali MAM (1979) Ecological and physiological studies on the alfalfa ladybird. Akadémiai Kiadó, Budapest
4. Álvarez-Alfageme F, Ferry N, Castañera P, Ortego F, Gatehouse AMR (2008) Prey mediated effects of Bt maize on fitness and digestive physiology of the red spider mite predator Stethorus punctillum Weise (Coleoptera: Coccinellidae). Transgenic Res 17:943–954
5. 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
6. Álvarez-Alfageme F, Pálinkás Z, Bigler F, Romeis J (2012) Development of an early-tier laboratory bioassay for assessing the impact of orally-active insecticidal compounds on larvae of Coccinella septempunctata (Coleoptera: Coccinellidae). Environ Entomol 41:1687–1693
7. Aragón P, Lobo JM (2012) Predicted effect of climate change on the invisibility and distribution of the Western corn root-worm. Agric For Entomol 14:13–18
8. Aragón P, Baselga A, Lobo JM (2010) Global estimation of invasion risk zones for the western corn rootworm Diabrotica virgifera virgifera: integrating distribution models and physiological thresholds to assess climatic favourability. J Appl Ecol 47:1026–1035
9. 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. Agric Ecosyst Environ 131:137–144
10. Biddinger DJ, Weber DC, Hull LA (2009) Coccinellidae as predators of mites: stethorini in biological control. Biol Control 51:268–283
11. Blümel S, Bakker FM, Baier B, Brown K, Candolfi MP, Goßmann A, Grimm C, Jäkel B, Nienstedt K, Schirra KJ, Ufer A, Waltersdorfer A (2000) Laboratory residual contact test with the predatory mite Typhlodromus pyri Scheuten (Acari: Phytoseiidae) for regulatory tesing of plant protection products. In: Candolfi MP, Blümel S, Forster R, Bakker FM, Grimm C, Hassan SA, Heimbach U, Mead-Briggs MA, Reber B, Schmuck R, Vogt H (eds) Guidelines to evaluate side-effects of plant protection products to non-target arthropods. IOBC/WPRS, Gent, pp 121–143
12. Bohan DA, Raybould A, Mulder C, Woodward G, Tamaddoni-Nezhad A, Bluthgen N, Pocock MJO, Muggleton S, Evans DM, Astegiano J, Massol F, Loeuille N, Petit S, Macfadyen S (2013) Networking agroecology: integrating the diversity of agroecosystem interactions. Adv Ecol Res 49:1–67
13. CAB International (2007) Crop protection compendium. Wallingford, UK
14. Carstens K, Cayabyab B, De Schrijver A, Gadaleta PG, Hellmich RL, Romeis J, Storer N, Valicente FH, Wach M (2014) Surrogate species selection for assessing potential adverse environmental impacts of genetically engineered insect-resistant plants on non-target organisms. GM Crops Food 5:1–5
15. COGEM (2013) Advisory report. Mixture toxicity regarding the application for cultivation of MON89034xNK603 maize (CGM/130604-02). http://www.cogem.net/index.cfm/en/publications/publicatie/advisory-report-mixture-toxicity-regarding-the-application-for-cultivation-of-mon89034xnk603-maize
16. Cortet J, Andersen MN, Caul S, Griffiths B, Joffre R, Lacroix B, Sausse C, Thompson J, Krogh PH (2006) Decomposition processes under Bt (Bacillus thuringiensis) maize: results of a multi-site experiment. Soil Biol Biochem 38:195–199
17. Council of the European Communities (1992) Council Directive 92/43/EEC of 21 May 1992 on the conservation of natural habitats and of wild fauna and flora. OJ L 206, 22.07.1992 flora. OJ L 206, 22.07.1992
18. De Schrijver A, Devos Y, Van den Bulcke M, Cadot P, De Loose M, Reheul D, Sneyers M (2007) Risk assessment of GM stacked events obtained from crosses between GM events. Trends Food Sci Technol 18:101–109
19. Devos Y, De Schrijver A, De Clercq P, Kiss J, Romeis J (2012) Bt-maize event MON 88017 expressing Cry3Bb1 does not cause harm to non-target organisms. Transgenic Res 21:1191–1214
20. Devos Y, Aguilera J, Diveki Z, Gomes A, Liu Y, Paoletti C, du Jardin P, Herman L, Perry JN, Waigmann E (2014) EFSA’s scientific activities and achievements on the risk assessment of genetically modified organisms (GMOs) during its first decade of existence: looking back and ahead. Transgenic Res 23:1–25
21. Edwards CR, Kiss J (2012) Diabrotica virgifera virgifera LeConte in Europe 2012. Based on data from country coordinators: E Cota (AL), G Grabenweger (AT), N Karic (BA), L Swillens (BE), I Ivanova (BG), Y Shymanskaya (BY), L Schaub & M Bertossa (CH), P Kroutil (CZ), P Baufeld (DE), JM Cobos (ES), B Huguet & M Delos (FR), S Ioannidou (GR), V Markoti (HR), G Ripka (HU), G Governatori (IT), B Pulaj (KS), RPJ Potting (NL), T Konefal (PL), M Cean (RO), I Sivcev (RS), (RU), G Urek (SI), J Kubik (SK), V Symonov & O Bashynska (UA), D Eyre (UK). http://extension.entm.purdue.edu/wcr/images/pdf/2012/EUROPEMap2012.pdf
22. EFSA (2010) Guidance on the environmental risk assessment of genetically modified plants. EFSA J 8(11):1879. http://www.efsa.europa.eu/it/scdocs/doc/1879.pdf
23. García M, Ortego F, Castañera P, Farinós GP (2012) Assessment of prey-mediated effects of the coleopteran-specific toxin Cry3Bb1 on the generalist predator Atheta coriaria (Coleoptera: Staphylinidae). Bull Entomol Res 102:293–302
24. Garcia-Alonso M, Raybould A (2013) Protection goals in environmental risk assessment: a practical approach. Transgenic Res. doi:10.1007/s11248-013-9760-1
25. Garcia-Alonso M, Jacobs E, Raybould A, Nickson TE, Sowig P, Willekens H, van der Kouwe P, Layton R, Amijee F, Fuentes AM, Tencalla F (2006) A tiered system for assessing the risk of genetically modified plants to non-target organisms. Environ Biosaf Res 5:57–65
26. Gray A (2012) Problem formulation in environmental risk assessment for genetically modified crops: a practitioner’s approach. Colln Biosaf Rev 6:10–65
27. Greathead D (1986) Parasitoids in biological control. In: Waage J, Greathead D (eds) Insect parasitoids. Academic Press, London, pp 289–318
28. Greenplate JT, Mullins JW, Penn SR, Dahm A, Reich BJ, Osborn JA, Rahn PR, Ruschke L, Shappley ZW (2003) Partial characterization of cotton plants expressing two toxin proteins from Bacillus thuringiensis: relative toxin contribution, toxin interaction, and resistance management. J Appl Entomol 127:340–347
29. Grimm C, Reber B, Barth M, Candolfi MP, Drexler A, Maus C, Moreth L, Ufer A, Waltersdorfer A (2000) A test for evaluating the chronic effects of plant protection products on the rove beetle Aleochara bilineata Gyll. (Coleoptera: Staphylinidae) under laboratory and extended laboratory conditions. In: Candolfi MP, Blümel S, Forster R, Bakker FM, Grimm C, Hassan SA, Heimbach U, Mead-Briggs MA, Reber B, Schmuck R, Vogt H (eds) Guidelines to evaluate side-effects of plant protection products to non-target arthropods. Belgium, IOBC/WPRS, pp 1–12
30. Heimbach U, Dohmen P, Barrett KL, Brown K, Kennedy PJ, Kleiner R, Römbke J, Schmitzer S, Schmuck R, Ufer A, Wilhelmy H (2000a) A method for testing effects of plant protection products on the carabid beetle Poecilus cupreus (Coleoptera: Carabidae) under laboratory and semi-field conditions. In: Candolfi MP, Blümel S, Forster R, Bakker FM, Grimm C, Hassan SA, Heimbach U, Mead-Briggs MA, Reber B, Schmuck R, Vogt H (eds) Guidelines to evaluate side-effects of plant protection products to non-target arthropods. IOBC/WPRS, Gent, pp 87–106
31. Heimbach U, Wehling A, Barrett KL, Candolfi MP, Jäckel B, Kennedy PJ, Mead-Briggs M, Nienstedt KM, Römbke J, Schmitzer S, Schmuck R, Ufer A, Wilhelmy H (2000b) A method for testing effects of plant protection products on spiders of the genus Pardosa (Araneae: Lycosidae) under laboratory conditions. In: Candolfi MP, Blümel S, Forster R, Bakker FM, Grimm C, Hassan SA, Heimbach U, Mead-Briggs MA, Reber B, Schmuck R, Vogt H (eds) Guidelines to evaluate side-effects of plant protection products to non-target arthropods. IOBC/WPRS, Gent, pp 71–86
32. Helsinki Commission (2013) Red List of Benthic Invertebrates, Species Information Sheet, Macroplea pubipennis. http://helcom.fi/Red%20List%20Species%20Information%20Sheet/HELCOM%20Red%20List%20Macroplea%20pubipennis.pdf
33. Herman RA, Scherer PN, Young DL, Mihaliak CA, Meade T, Woodsworth AT, Stockhoff BA, Narva KE (2002) Binary insecticidal crystal protein from Bacillus thuringiensis, strain PS149B1: effects of individual protein components and mixtures in laboratory bioassays. J Econ Entomol 95:635–639
34. Hodek I (1996) Food relationships. In: Hodek I, Honěk A (eds) Ecology of Coccinellidae. Kluwer, Dordrecht, pp 143–238
35. Hodek I, Evans EW (2012) Food relationships. In: Hodek I, van Emden HF, Honěk A (eds) Ecology and behaviour of the Ladybird Beetles (Coccinellidae). Blackwell, Chichester, pp 141–274
36. Holst N, Lang A, Lövei G, Otto M (2013) Increased mortality is predicted of Inachis io larvae caused by Bt-maize pollen in European farmland. Ecol Model 250:126–133
37. Huesing JE, Romeis J, Ellstrand NC, Raybould A, Hellmich RL, Wolt JD, Ehlers JD, Dabiré-Binso LC, Fatokun CA, Hokanson KE, Ishiyaku MF, Margam VM, Obokoh N, Mignouna JD, Nang’ayo F, Ouedraogo JT, Pasquet RS, Pittendrigh BR, Schaal BA, Stein J, Tamò M, Murdock LL (2011) Regulatory considerations surrounding the deployment of Bt-expressing cowpea in Africa. GM Crops 2:211–224
38. James C (2013) Global status of commercialized biotech/GM crops: 2013. ISAAA Brief 46. ISAAA, Ithaca
39. Keller I, Fluri P, Imdorf A (2005) Pollen nutrition and colony development in honey bees: part I. Bee World 86:3–10
40. Kiss J (1989) Comparison of directional light trap catches in maize. Bull Univ Agric Sci Gödöllö 1:73–80
41. Knecht S, Nentwig W (2010) Effect of Bt maize on the reproduction and development of saprophagous Diptera over multiple generations. Basic Appl Ecol 11:346–353
42. Kotze DJ, Brandmayr P, Casale A, Dauffy-Richard E, Dekoninck W, Koivula MJ, Lövei GL, Mossakowski D, Noordijk J, Paarmann W, Pizzolotto R, Saska P, Schwerk A, Serrano J, Szyszko J, Taboada A, Turin H, Venn S, Vermeulen R, Zetto T (2011) Forty years of carabid beetle research in Europe—from taxonomy, biology, ecology and population studies to bioindication, habitat assessment and conservation. ZooKeys 100:55–148
43. Krupke CH, Hunt GJ, Eitzer BD, Andino G, Given K (2012) Multiple routes of pesticide exposure for honey bees living near agricultural fields. PLoS ONE 7:e29268
44. 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
45. Li H, Olson M, Lin G, Hey T, Tan SY, Narva KE (2013) Bacillus thuringiensis Cry34Ab1/Cry35Ab1 interactions with western corn rootworm midgut membrane binding sites. PLoS ONE 8:e53079
46. Lisowicz F (1989) Xylena vetusta Hb. (Lep., Noctuidae, Cucullianae), a new pest of maize in Poland. Acta Phytopathol Entomol Hung 4:145–146
47. Ludy C, Lang A (2006) Bt maize pollen exposure and impact on the garden spider, Araneus diadematus. Entomol Exp Appl 118:145–156
48. Meissle M, Romeis J (2009) The web-building spider Theridion impressum (Araneae: Therididae) is not adversely affected by Bt maize resistant to corn rootworms. Plant Biotechnol J 7:645–656
49. 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
50. Meissle M, Mouron P, Musa T, Bigler F, Pons X, Vasileiadis VP, Otto S, Antichi D, Kiss J, Pálinkás Z, Dorner Z, van der Weide R, Groten J, Czembor E, Adamczyk J, Thibord J-B, Melander B, Nielsen GC, Poulsen RT, Zimmermann O, Verschwele A, Oldenburg E (2010) Pests, pesticide use and alternative options in European maize production: current status and future prospects. J Appl Entomol 134:357–375
51. Meissle M, Romeis J, Bigler F (2011) Bt maize and integrated pest management—a European perspective. Pest Manag Sci 67:1049–1058
52. Meissle M, Álvarez-Alfageme F, Malone LA, Romeis J (2012) Establishing a database of bio-ecological information on non-target arthropod species to support the environmental risk assessment of genetically modified crops in the EU. Supporting Publications 2012: EN-334. European Food Safety Authority (EFSA), Parma. http://www.efsa.europa.eu/en/supporting/pub/334e.htm
53. Mulder C, Ahrestani FS, Bahn M, Bohan DA, Bonkowski M, Griffiths BS, Guicharnaud RA et al (2013) Connecting the green and brown worlds: allometric and stoichiometric predictability of above- and below-ground networks. Adv Ecol Res 49:69–175
54. Mullin CA, Saunders MC, Leslie TW, Biddinger DJ, Fleischer SJ (2005) Toxic and behavioural effects to Carabidae of seed treatments used on Cry3Bb1- and Cry1Ab/c-protected corn. Environ Entomol 34:1626–1636
55. Nienstedt KM, Brock TCM, van Wensem J, Montforts M, Hart A, Aagaard A, Alix A, Boesten J, Bopp SK, Brown C, Capri E, Forbes V, Köpp H, Liess M, Luttik R, Maltby L, Sousa JP, Streissl F, Hardy AR (2012) Development of a framework based on an ecosystem services approach for deriving specific protection goals for environmental risk assessment of pesticides. Sci Total Environ 415:31–38
56. Obrist LB, Dutton A, Albajes R, Bigler F (2006a) Exposure of arthropod predators to Cry1Ab toxin in Bt maize fields. Ecol Entomol 31:143–154
57. Obrist LB, Klein H, Dutton A, Bigler F (2006b) Assessing the effects of Bt maize on the predatory mite Neoseiulus cucumeris. Exp Appl Acarol 38:125–139
58. OECD (1998) OECD series on principles of good laboratory practice and compliance monitoring. Organisation for Economic Co-operation and Development, Paris. http://www.oecd.org/document/63/0,3343,en_2649_34381_2346175_1_1_1_1,00.html
59. 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. http://www.epa.gov/oppbppd1/biopesticides/pips/reg-biotech.pdf
60. Perry JN, Devos Y, Arpaia S, Bartsch D, Gathmann A, Hails RS, Kiss J, Lheureux K, Manachini B, Mestdagh S, Neemann G, Ortego F, Schiemann J, Sweet JB (2010) A mathematical model of exposure of non-target Lepidoptera to Bt-maize pollen expressing Cry1Ab within Europe. Proc R Soc B Biol Sci 277:1417–1425
61. Perry JN, Devos Y, Arpaia S, Bartsch B, Ehlert C, Gathmann A, Hails RS, Hendriksen NB, Kiss J, Messéan A, Mestdagh S, Neemann G, Nuti M, Sweet JB, Tebbe CC (2012) Estimating the effects of Cry1F Bt-maize pollen on non-target Lepidoptera using a mathematical model of exposure. J Appl Ecol 49:29–37
62. Perry JN, Arpaia S, Bartsch B, Birch ANE, Devos Y, Gathmann A, Gennaro A, Kiss J, Messéan A, Mestdagh S, Nuti M, Sweet JB, Tebbe CC (2013) No evidence requiring change in the risk assessment of Inachis io larvae. Ecol Model 268:103–122
63. Peter M, Lindfeld A, Nentwig W (2010) Does GM wheat affect saprophagous Diptera species (Drosophilidae, Phoridae)? Pedobiologia 53:271–279
64. Peterson RKD, Meyer SJ, Wolf AT, Wolt JD, Davis PM (2006) Genetically engineered plants, endangered species, and risk: a temporal and spatial exposure assessment for Karner blue butterfly larvae and Bt maize pollen. Risk Anal 26:845–858
65. Peterson JA, Obrycki JJ, Harwood JD (2009) Quantification of Bt-endotoxin exposure pathways in carabid food webs across multiple transgenic events. Biocontrol Sci Technol 19:613–625
66. Porcar M, García-Robles I, Domínguez-Escribà L, Latorre A (2010) Effects of Bacillus thuringiensis Cry1Ab and Cry3Aa endotoxins on predatory Coleoptera tested through artificial diet-incorporation bioassay. Bull Entomol Res 100:297–302
67. Priesnitz K-U, Benker U, Schaarschmidt F (2013) Assessment of the potential impact of a Bt maize hybrid expressing Cry3Bb1 on ground beetles (Carabidae). J Plant Dis Prot 120:131–140
68. Quince C, Higgs PG, McKane AJ (2005) Deleting species from model food webs. Oikos 110:283–296
69. Raybould A (2006) Problem formulation and hypothesis testing for environmental risk assessments of genetically modified crops. Environ Biosaf Res 5:119–125
70. Raybould A, Vlachos D (2011) Non-target organism effects tests on Vip3A and their application to the ecological risk assessment for cultivation of MIR162 maize. Transgenic Res 20:599–611
71. Raybould A, Stacey D, Vlachos D, Graser G, Li X, Joseph R (2007) Non-target organism risk assessment of MIR604 maize expressing mCry3A for control of corn rootworm. J Appl Entomol 131:391–399
72. Raybould A, Graser G, Hill K, Ward K (2011) Ecological risk assessments for transgenic crops with combined insect-resistance traits: the example of Bt11 × MIR604 maize. J Appl Entomol 136:27–37
73. Römbke J (2006) Tools and techniques for the assessment of ecotoxicological impacts of contaminants in the terrestrial environment. Hum Ecol Risk Assess 12:84–101
74. Romeis J, Meissle M (2011) Non-target risk assessment of Bt crops—cry protein uptake by aphids. J Appl Entomol 135:1–6
75. 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
76. Romeis J, Hellmich RL, Candolfi MP, Carstens K, De Schrijver A, Gatehouse AMR, Herman RA, Huesing JE, McLean MA, Raybould A, Shelton AM, Waggoner A (2011) Recommendations for the design of laboratory studies on non-target arthropods for risk assessment of genetically engineered plants. Transgenic Res 20:1–22
77. Romeis J, Raybould A, Bigler F, Candolfi MP, Hellmich RL, Huesing JE, Shelton AM (2013) Deriving criteria to select arthropod species for laboratory tests to assess the ecological risks from cultivating arthropod-resistant genetically engineered crops. Chemosphere 90:901–909
78. Rose RI (ed) (2007) White paper on tier-based testing for the effects of proteinaceous insecticidal plant-incorporated protectants on non-target invertebrates for regulatory risk assessment. USDA-APHIS and US Environmental Protection Agency, Washington DC. http://www.epa.gov/pesticides/biopesticides/pips/non-target-arthropods.pdf
79. Sanvido O, Romeis J, Bigler F (2009) An approach for post-market monitoring of potential environmental effects of Bt-maize expressing Cry1Ab on natural enemies. J Appl Entomol 133:236–248
80. Sanvido O, Romeis J, Gathmann A, Gielkens M, Raybould A, Bigler F (2012) Evaluating environmental risks of genetically modified crops—ecological harm criteria for regulatory decision-making. Environ Sci Policy 15:82–91
81. Schmitz G, Bartsch D, Pretscher P (2003) Selection of relevant non-target herbivores for monitoring the environmental effects of Bt maize pollen. Environ Biosaf Res 2:117–132
82. Schmuck R, Candolfi MP, Kleiner R, Mead-Briggs M, Moll M, Kemmeter F, Jans D, Waltersdorfer A, Wilhelmy H (2000) A laboratory test system for assessing effects of plant protection products on the plant dwelling insect Coccinella septempunctata L. (Coleoptera: Coccinellidae). In: Candolfi MP, Blümel S, Forster R, Bakker FM, Grimm C, Hassan SA, Heimbach U, Mead-Briggs MA, Reber B, Schmuck R, Vogt H (eds) Guidelines to evaluate side-effects of plant protection products to non-target arthropods. IOBC/WPRS, Belgium, pp 45–56
83. Schuppener M, Mühlhause J, Müller A-K, Rauschen S (2012) 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. Mol Ecol 21:4646–4662
84. Solé RV, Montoya JM (2001) Complexity and fragility in ecological networks. Proc R Soc B Biol Sci 268:2039–2045
85. Stacey D, Graser G, Mead-Briggs M, Raybould A (2006) Testing the impact on non-target organisms of insecticidal proteins expressed in transgenic crops. IOBC/WPRS Bull 29:165–172
86. Turian G (1969) Coccinelles micomycétophages (Col.). Mit Schweiz Entomol Ges 42:52–57
87. Van Lenteren JC (2012) The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. Biocontrol 57:1–20
88. van Swaay C, Cuttelod A, Collins S, Maes D, Munguira ML, Šašić M, Settele J, Verovnik R, Verstrael T, Warren M, Wiemers M, Wynhoff I (2010) European red list of butterflies. Publications Office of the European Union, Luxembourg. http://ec.europa.eu/environment/nature/conservation/species/redlist/downloads/European_butterflies.pdf
89. Vasileiadis VP, Sattin M, Otto S, Veres A, Pálinkás Z, Ban R, Pons X, Kudsk P, van der Weide R, Czembor E, Moonen AC, Kiss J (2011) Crop protection in European maize-based cropping systems: current practices and recommendations for innovative integrated pest management. Agric Syst 104:533–540
90. 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
91. Weber G, Prescher S (1995) Die Mücken und Fliegen eines klärschlammgedüngten Ackers. Agrarökologie 15:1–100
92. Wesseler J, Fall EH (2010) Potential damage costs of Diabrotica virgifera virgifera infestation in Europe—the ‘no control’. J Appl Entomol 134:385–394
93. Wolt JD, Conlan CA, Majima K (2005) An ecological risk assessment of Cry1F maize pollen impact to pale grass blue butterfly. Environ Biosaf Res 4:243–251
94. Wolt JD, Keese P, Raybould A, Fitzpatrick JW, Burachik M, Gray A, Olin SS, Schiemann J, Sears M, Wu F (2010) Problem formulation in the environmental risk assessment for genetically modified plants. Transgenic Res 19:425–436
95. Zurbrügg C, Hönemann L, Meissle M, Romeis J, Nentwig W (2010) Decomposition dynamics and structural plant components of genetically modified Bt maize leaves do not differ from leaves of conventional hybrids. Transgenic Res 19:257–267
96. Zwahlen C, Andow DA (2005) Field evidence for the exposure of ground beetles to Cry1Ab from transgenic corn. Environ Biosaf Res 4:113–117