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Monitoring the impact of Bt maize on butterflies in the field: estimation of required sample sizes

Published online by Cambridge University Press:  15 March 2004

Andreas Lang*
Affiliation:
Bavarian State Research Centre for Agriculture, Institute of Plant Protection, Lange Point 10, 85354 Freising, Germany

Abstract

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The monitoring of genetically modified organisms (GMOs) after deliberate release is important in order to assess and evaluate possible environmental effects. Concerns have been raised that the transgenic crop, Bt maize, may affect butterflies occurring in field margins. Therefore, a monitoring of butterflies was suggested accompanying the commercial cultivation of Bt maize. In this study, baseline data on the butterfly species and their abundance in maize field margins is presented together with implications for butterfly monitoring. The study was conducted in Bavaria, South Germany, between 2000–2002. A total of 33 butterfly species was recorded in field margins. A small number of species dominated the community, and butterflies observed were mostly common species. Observation duration was the most important factor influencing the monitoring results. Field margin size affected the butterfly abundance, and habitat diversity had a tendency to influence species richness. Sample size and statistical power analyses indicated that a sample size in the range of 75 to 150 field margins for treatment (transgenic maize) and control (conventional maize) would detect (power of 80%) effects larger than 15% in species richness and the butterfly abundance pooled across species. However, a much higher number of field margins must be sampled in order to achieve a higher statistical power, to detect smaller effects, and to monitor single butterfly species.

Type
Research Article
Copyright
© ISBR, EDP Sciences, 2004

References

Barrett KL, Grandy N, Harrison EG, Hassan SA, Oomen PA, eds (1994) Guidance document on regulatory testing procedures for pesticides and non-target arthropods. SETAC Europe, Brussels
Bayerisches Landesamt für Umweltschutz (2003) Entwurf zur Neufassung der Roten Liste der Tagfalter (Lepidoptera: Rhopalocera) Bayerns. Unpublished report of the Bavarian Environmental Protection Agency (LfU)
Bourguet D, Chaufaux J, Micoud A, Delos M, Naibo B, Bombarde F, Marque G, Eychenne N, Pagliari C (2002) Ostrinia nubilalis parasitism and the field abundance of non-target insects in transgenic Bacillus thuringiensis corn (Zea mays). Environ. Biosafety Res. 1: 49–60
Brunzel S, Plachter H (1999) Bewerten mit Tagfaltern im Naturschutz. In Settele J, Feldmann R, Reinhardt R, eds, Die Tagfalter Deutschlands. Eugen Ulmer, Stuttgart, pp 186–213
Chazdon RL, Colwell RK, Denslow JS, Guariguata MR (1998) Statistical methods for estimating species richness of woody regeneration in primary and secondary rain forests of NE Costa Rica. In Dallmeier F, Comiskey JA, eds, Forest biodiversity research, monitoring and modeling: Conceptual background and Old World case studies. Parthenon Publishing, Paris. pp 285–309
Collinge SK, Prudic KL, Oliver JC (2003) Effects of local habitat characteristics and landscape context on grassland butterfly diversity. Conserv. Biol. 17: 178–187
Colwell RK (1997) EstimateS: Statistical estimation of species richness and shared species from samples. Version 5. User’s Guide and application published at: http://viceroy.eeb.uconn.edu/estimates
Colwell, RK, Coddington, JA (1994) Estimating terrestrial biodiversity through extrapolation. Phil. Trans. R. Soc. Lond. B. 345: 101118 CrossRef
Connor EF, McCoy ED (1979) The statistics and biology of the species-area relationship. Am. Nat. 113: 791–833
Conner, AJ, Glare, TR, Nap, J-P (2003) The release of genetically modified crops into the environment. Part II. Overview of ecological risk assessment. Plant J. 33: 1946 CrossRef
Dennis RLH, Shreeve TG (1997) Diversity of butterflies on British islands: ecological influences underlying the roles of area, isolation and the size of the faunal source. Biol. J. Linn. Soc. 60: 257–275
Diamond E (2003) Science as a smokescreen? A report on the farm scale evaluations of GM herbicide tolerant crops. Report to the Friends of the Earth (FOE), England, published at: http://www.foe.co.uk/resource/reports/science_smokescreen.pdf, May 19, 2003
Dutton A, Romeis J, Bigler F (2003) Test procedure to evaluate the risk that insect-resistant transgenic plants pose to entomophagous arthropods. In Van Driesche RG, ed, Proceedings of the First International Symposium on Biological Control of Arthropods, Honolulu, Hawaii, 14–18 Jan. 2002, United States Department of Agriculture, Forest Service, Morgantown, WV, FHTET-2003-05, pp 466–472
Ebert G, Rennwald E (1991a) Die Schmetterlinge Baden-Württembergs. Band 1: Tagfalter I. Eugen Ulmer, Stuttgart
Ebert G, Rennwald E (1991b) Die Schmetterlinge Baden-Württembergs. Band 2: Tagfalter II. Eugen Ulmer, Stuttgart
European Parliament and Council (2001) Directive 2001/18/EC of the European Parliament and of the Council of 12 March 2001 on the deliberate release into the environment of genetically modified organisms and repealing Council Directive 90/220/EC – Commission Declaration. Official Journal L 106: 1–39
Feber RE, Smith H, Macdonald DW (1996) The effects on butterfly abundance of the management of uncropped edges of arable fields. J. Appl. Ecol. 33: 1191–1205
Feber, RE, Smith, H, Macdonald, DW (1999) The importance of spatially variable field margin management for two butterfly species. Asp. Appl. Biol. 54: 155162
Feber RE, Firbank LG, Johnson PJ, Macdonald DW (1997) The effects of organic farming on pest and non-pest butterfly abundance. Agric. Ecosys. Environ. 64: 133–139
Felke M, Langenbruch GA (2001) Gefährdet Bt-Pollen Schmetterlinge? Ges. Pflanzen 53: 24–28
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. Ent. 126: 320–325
Firbank LG, Heard MS, Woiwod IP, Hawes C, Haughton AJ, Champion GT, Scott RJ, Hill MO, Dewar AM, Squires GR, May MJ, Brooks DR, Bohan DA, Daniels RE, Osborne JL, Roy DB, Black HIJ, Rothery P, Perry JN (2003) An introduction to the Farm-Scale Evaluations of genetically modified herbicide-tolerant crops. J. Appl. Ecol. 40: 2–16
Gutiérrez, D, Thomas, CD, Léon-Cortés, JL (1999) Dispersal, distribution, patch network and metapopulation dynamics of the dingy skipper butterfly (Erynnis tages). Oecologia 121: 506517
Hansen Jesse LC, Obrycki JJ (2000) Field deposition of Bt transgenic corn pollen: lethal effects on the monarch butterfly. Oecologia 125: 241–248
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. Nat. Acad. Sci. USA 98: 1192511930 CrossRef
Hermann G (1992) Tagfalter und Widderchen – Methodisches Vorgehen bei Bestandsaufnahmen zu Naturschutz- und Eingriffsplanungen. In Trautner J., ed, Arten und Biotopschutz in der Planung: Methodische Standards zur Erfassung von Tierartengruppen. Margraf, Weikersheim, pp 219–238
Hermann G (1999) Methoden der qualitativen Erfassung von Tagfaltern. In Settele J, Feldmann R, Reinhardt R, eds, Die Tagfalter Deutschlands. Eugen Ulmer, Stuttgart, pp 124–143
Hodgson JG (1993) Commonness and rarity in British butterflies. J. Appl. Ecol. 30: 407–427
Jepson PC, Croft BA, Pratt GE (1994) Test systems to determine the ecological risks posed by toxin release from Bacillus thuringiensis genes in crop plants. Mol. Ecol. 3: 81–89
Johnson KS, Scriber JM, Nitao JK, Smitley DR (1995) Toxicity of Bacillus thuringiensis var. kurstaki to three nontarget Lepidoptera in field studies. Environ. Entomol. 24: 288–297
Kruess A, Tscharntke T (2002) Grazing intensity and the diversity of grasshoppers, butterflies, and trap-nesting bees and wasps. Conserv. Biol. 16: 1570–1580
Lang A, Abdel-Kader K, Arndt M, Bauchhenß J, Beck R, Benker U, Herrmann A, Mautz D, Zellner M, Pommer G (2004) Monitoring der Umweltwirkungen von Bt-Mais. Ein Forschungsprojekt des Bayerischen Staatsministeriums für Landesentwicklung und Umweltfragen und der Bayerischen Landesanstalt für Landwirtschaft. Mitt. BBA, in press
Losey JE, Rayor LS, Carter ME (1999) Transgenic pollen harms monarch larvae. Nature 399: 214
Luff ML (2002) Carabid assemblage organization and species composition. In Holland JM, ed, The Agroecology of Carabid Beetles, Intercept, Andover, pp 41–79
Lövei GL (2001) Ecological risks and benefits of transgenic plants. Proc. New Zealand Plant Protect. Conf. 54: 93–100
MacArthur R, Wilson EO (1967) The theory of island biogeography. Princeton University Press, Princeton, N.J.
Miller JC (1990) Field assessment of the effects of a microbial pest control agent on nontarget Lepidoptera. Am. Entomol. 26: 135–139
Mühlhofer G (1999) Tagfalter. In Schlumprecht H, ed, Handbuch landschaftsökologischer Leistungen. Veröffentlichungen der VUBD, Band 1. VUBD, Nürnberg, pp 248–257
Munguira, ML, Thomas, JA (1992) Use of road verges by butterfly and burnet populations, and the effect of roads on adult dispersal and mortality. J. Appl. Ecol. 29: 316329 CrossRef
Nap J-P, Metz PL, Escaler M, Conner AJ (2003) The release of genetically modified crops into the environment. Part I. Overview of current status and regulations. Plant J. 33: 1–18
Niemelä J, Baur B (1998) Threatened species in a vanishing habitat: plants and invertebrates in calcareous grasslands in the Swiss Jura mountains. Biodiv. Conserv. 7: 1407–1416
Perry, JN, Rothery, P, Clark, SJ, Heard, MS, Hawes, C (2003) Design, analysis and statistical power of the Farm-Scale Evaluations of genetically modified herbicide-tolerant crops. J. Appl. Ecol. 40: 1731 CrossRef
Pleasants, JM, Hellmich, RL, Dively, GP, Sears, MK, Stanley-Horn, DE, Mattila, HR, Foster, JE, Clark, TL, Jones, GD (2001) Corn pollen deposition on milkweeds in and near corn fields. Proc. Nat. Acad. Sci. USA 98: 1191911924 CrossRef
Pretscher P (1998) Rote Liste der Großschmetterlinge (Macrolepidoptera). Tagfalter (Rhopalocera) einschließlich Dickkopffalter (Hesperiidae). In Bundesamt für Naturschutz, ed, Rote Liste gefährdeter Tiere Deutschlands. Landwirtschaftsverlag GmbH, Münster-Hiltrup, pp 87–98
Pollard E (1977) A method for assessing changes in the abundance of butterflies. Biol. Conserv. 12: 115–134
Pollard E (1984) Fluctuations in the abundance of butterflies, 1976–1982. Ecol. Entomol. 9: 179–188
Samu F, Szinetár C (2002) On the nature of agrobiont spiders. J. Arachnol. 30: 389–402
Schmitz G, Bartsch D, Pretscher P (2003) Selection of relevant non-target herbivores for monitoring the environmental effects of Bt maize pollen. Environ. Biosafety Res. 2: 117–132
Schneider C, Dover J, Fry GLA (2003) Movement of two grassland butterflies in the same habitat network: the role of adult resources and size of the study area. Ecol. Entomol. 28: 219–227
Settele J, Feldmann R, Henle K, Kockelke K, Poethke H-J (1999) Methoden der quantitativen Erfassung von Tagfaltern. In Settele J, Feldmann R, Reinhardt R, eds, Die Tagfalter Deutschlands. Eugen Ulmer, Stuttgart, pp 144–185
Stanley-Horn DE, Dively GP, Hellmich RL, Mattila HR, Sears MK, Rose R, Hansen Jesse LC, Losey JE, Obrycki JJ, Lewis L (2001) Assessing the impact of Cry1Ab-expressing corn pollen on monarch butterfly larvae in field studies. Proc. Nat. Acad. Sci. USA 98: 11931–11936
Steffan-Dewenter I, Tscharntke T (1997) Early succession of butterfly and plant communities on set-aside fields. Oecologia 109: 294–302
Steffan-Dewenter I, Tscharntke T (2000) Butterfly community structure in fragmented habitats. Ecol. Letters 3: 449–456
Summerville KS, Crist TO (2001) Effects of experimental habitat fragmentation on patch use by butterflies and skippers (Lepidoptera). Ecology 85: 1360–1370
Tischler W (1958) Synökologische Untersuchungen an der Fauna der Felder und Feldgehölze. Z. Morph. Ökol. Tiere 47: 54–114
Tolman T, Lewington R (1998) Die Tagfalter Europas und Nordwestafrikas. Franckh-Kosmos, Stuttgart
Thomas CD, Harrison S (1992) Spatial dynamics of a patchily distributed butterfly species. J. Anim. Ecol. 61: 437–446
Thomas JA, Bourn NAD, Clarke RT, Stewart KE, Simcox DJ, Pearman GS, Curtis R, Goodger B (2001) The quality and isolation of habitat patches both determine where butterflies persist in fragmented landscapes. Proc. R. Soc. Lond. B 268: 1791–1796
Van Rie J (2000) Bacillus thuringiensis and its use in transgenic insect control technologies. Int. J. Med. Microbiol. 290: 463–469
Villiger M (1999) Effekte transgener insektenresistenter Bt-Kulturpflanzen auf Nichtzielorganismen am Beispiel der Schmetterlinge. WWF Schweiz, Zürich
Wagner DL, Peacock JW, Carter JL, Talley SE (1996) Field assessment of Bacillus thuringiensis on nontarget Lepidoptera. Environ. Entomol. 25: 1444–1454
Weibull A-C, Bengtsson J, Nohlgren E (2000) Diversity of butterflies in the agricultural landscape: the role of farming system and landscape heterogeneity. Ecography 23: 743–750
Wilhelm, R, Beißner, L, Schiemann, J (2002) Gestaltung des Monitoring der Auswirkungen gentechnisch veränderter Pflanzen im Agrarökosystem. Ges. Pflanzen 54: 194206 CrossRef
Wraight CL, Zangerl AR, Carroll MJ, Berenbaum MR (2000) Absence of toxicity of Bacillus thuringiensis pollen to black swallowtails under field conditions. Proc. Nat. Acad. Sci. USA 97: 7700–7703
Zangerl AR, McKenna D, Wraight CL, Carroll M, Ficarello P, Warner R, Berenbaum MR (2001) Effects of exposure to event 176 Bacillus thuringiensis corn pollen on monarch and black swallowtail caterpillars under field conditions. Proc. Nat. Acad. Sci. USA 98: 11908–11912
Züghart W, Breckling B (2003) Konzeptionelle Entwicklung eines Monitoring von Umweltwirkungen transgener Kulturpflanzen. UBA-Texte 50/2003