Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-11T07:39:39.771Z Has data issue: false hasContentIssue false

Spatial distribution of Aglais urticae (L.) and its host plant Urtica dioica (L.) in an agricultural landscape: implicationsfor Bt maize risk assessment and post-market monitoring

Published online by Cambridge University Press:  19 September 2006

Achim Gathmann
Affiliation:
Aachen University, Institute of Environmental Research, Chair of Ecology, Ecotoxicology and Ecochemistry, Worringerweg 1, 52062 Aachen, Germany
Ludger Wirooks
Affiliation:
Steinkaulstr. 46, 52070 Aachen, Germany
Jörg Eckert
Affiliation:
Aachen University, Institute of Environmental Research, Chair of Ecology, Ecotoxicology and Ecochemistry, Worringerweg 1, 52062 Aachen, Germany
Ingolf Schuphan
Affiliation:
Aachen University, Institute of Environmental Research, Chair of Ecology, Ecotoxicology and Ecochemistry, Worringerweg 1, 52062 Aachen, Germany

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Over the past decades, genes of Bacillus thuringiensis var. kurstaki (Berliner) (Bt) coding for protein toxins have been engineered into maize for protection against the European Corn Borer (Ostrinia nubilalis (Hbn.)). However, these transgenic plants may have an impact on non-target organisms. In particular, a potential hazard was identified for non-target lepidopteran larvae, if they consume Bt maize pollen on their host plants. Risk can be defined as a function of the effect of an event (hazard) and the likelihood of this event occurring. Although data on toxicity (hazard) are available from many lab and field studies, knowledge about the environmental exposure of European lepidopteran larvae is incomplete at the population level. Therefore we studied the distribution of small tortoiseshell caterpillars (Aglais urticae (L.)) and its host plant in an agricultural landscape in Germany, to estimate the potential population exposure to maize pollen. The results showed that larvae of the small tortoiseshell developed primarily on freshly sprouted nettle stands (Urtica dioica (L.)) in field margins, rather than adjacent to hedges and groves. However, the main distribution was at margins of cereal (non-maize) fields, where 70% of all larvae were found. This may be due the fact that cereals covered 54% of the survey area, while maize only covered 6.1%. On the other hand, maize fields seem so show higher food plant densities than cereal crops. The results must be interpreted carefully, as the data basis of the present study is very small, and the situation can vary between years due to crop rotation or other changes in agricultural practices. Therefore it is still questionable whether the small tortoiseshell is significantly exposed to maize pollen. For a conclusive risk assessment, more replications and surveys of larger areas in different intensively managed agricultural landscapes over several years are needed.

Type
Research Article
Copyright
© ISBR, EDP Sciences, 2006

References

Boatman N (1994) Field Margins: Integrating Agriculture and Conservation. BCBP
Bryant, SR, Thomas, CD, Bale, JS (1997) Nettle feeding nymphalid butterflies: temperature, development and distribution. Ecol. Entomol. 22: 390398 CrossRef
Caldow, RWG, Racey, PA (2000) Large Scale Processes in Ecology and Hydrology. J. Appl. Ecol. 37: 18 CrossRef
Dale, PJ, Clarke, B, Fontes, EMD (2002) Potential for the environmental impact of transgenic crops. Nat. Biotechnol. 20: 567574 CrossRef
Davis, BNK, Lakhani, KH, Yates, TJ (1991) The hazards of insecticides to butterflies of field margins. Agr. Ecosyst. Environ. 36: 151161 CrossRef
den Nijs HCN, Bartsch D (2004) Introgression of GM plants and the EU guidance note for monitoring. In den Nijs HCN, Bartsch D, Sweet J, eds, Introgression from genetically modified plants into wild relatives, CABI Publishing Cambridge, pp 365–389
Dively, GP, Rose, R, Sears, MK, Hellmich, RL, Stanley-Horn, DDE, Calvin, DD, Russo, JM, Anderson, PL (2004) Effects on Monarch butterfly larvae (Lepidoptera: Danaidae) after continuous exposure to Cry1Ab-expressing corn during anthesis. Environ. Entomol. 33: 11161125 CrossRef
Ebert G, Rennwald E (1991) A. urticae. In Ebert G, Rennwald E, eds, Die Schmetterlinge Baden-Württembergs, Band 1, Tagfalter I. Verlag Eugen Ulmer, Stuttgart, pp 391–398
EFSA (2005a) Opinion of the Scientific Panel on Genetically Modified Organisms on a request from the Commission related to the notification (Reference C/F/96/05.10) for the placing on the market of insect-tolerant genetically modified maize Bt11, for cultivation, feed and industrial processing, under Part C of Directive 2001/18/EC from Syngenta Seeds. EFSA J. 213: 133
EFSA (2005b) Opinion of the Scientific Panel on Genetically Modified Organisms on a request from the Commission related to the notification (Reference C/ES/01/01) for the placing on the market of insect-tolerant genetically modified maize 1507, for import, feed and industrial processing and cultivation, under Part C of Directive 2001/18/EC from Pioneer Hi-Bred International/Mycogen Seeds. EFSA J. (2005) 181: 1–33
Eitschberger, U, Reinhardt, R, Steiniger, H (1991) Wanderfalter in Europa (Lepidoptera) – Appeal of International Cooperation in the Research of the Migration of Insects. Atalanta 22: 1833
Evans HF (2002) Environmental Impact of Bt Exudates from Roots of Genetically Modified Plants. Defra-Report (EPG 1/5/156). http://www.defra.gov.uk/environment/gm/research/pdf/epg_1-5-156.pdf
Felke, M, Langenbruch, G-A (2005) Auswirkungen des Pollens von transgenem Bt-Mais auf ausgewählte Schmetterlingslarven. BfN-Skripten 157: 1143
Felke, M, Lorenz, N, Langenbruch, G-A (2002) Laboratory studies on the effects of pollen from Bt-maize on larvae of some butterfly species. J. Appl. Entomol. 126: 320– 325 CrossRef
Firbanks, LG, Heard, MS, Woiwod, IP, Hawes, C, Haughton, AJ, Champion, GT, Scott, RJ, Hill, MO, Dewar, AM, Squire, 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: 216 CrossRef
Gathmann, A, Wirooks, L, Hothorn, LA, Schuphan, I (2006) Impact of Bt-pollen (MON810) on lepidopteran larvae living on accompanying weeds. Mol. Ecol. 15: 2677-2685 CrossRef
Hausmann, A (1990) Zur Dynamik von Nachtfalter-Artenspektren: Turnover und Dispersionsverhalten als Elemente von Verbreitungsstrategien. Spixiana Suppl. 16: 1222
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 thurningiensis-purified proteins and pollen. Proc. Natl. Acad. Sci USA 98: 1192511930 CrossRef
Hensle, J (2004) Papilionidae, Pieridae, Nymphalidae und Lycaenidae 2004. Atalanta 36: 1586
Jeanneret, P, Schüpbach, B, Pfiffner, L, Walter, T (2003) Arthropod reaction to landscape and habitat features in agricultural landscapes. Landscape Ecol. 18: 253263 CrossRef
Jepson, PC, Croft, BA, Pratt, GE (1994) Test systems to determine the ecological risks by toxin release from Bacillus thuringiensis genes in crop plants. Mol. Ecol. 3: 8189 CrossRef
Jesse, LCH, Obrycki, JJ (2002) Assessment of the non-target effects of transgenic Bt corn pollen and anthers on the milkweed tiger moth Euchatias egle Drury (Lepidoptera: Arctiidae). J. Kansas Entomol. Soc. 75: 5558
Krauss, J, Dewnter-Steffan, I, Tscharntke, T (2003) Local species immigration, extinction, and turnover of butterflies in relation to habitat area and habitat isolation. Oecologia 442: 591602 CrossRef
Lang, A (2004) Monitoring the impact of Bt maize on butterflies in the field: estimation of required sample sizes. Environ. Biosafety Res. 3: 5566 CrossRef
Lang, A, Ludy, C, Vojtech, E (2004) Dispersion and deposition of Bt maize pollen in field margins. J. Plant Dis. Prot. 111: 417428
Longely, M, Sotherton, N (1997) Factors determining the effects of pesticides upon butterflies inhabiting arable farmland. Agr. Ecosyst. Environ. 61: 112 CrossRef
Losey, JE, Rayor, LS, Carter, ME (1999) Transgenic pollen harms monarch larvae. Nature 399: 214 CrossRef
Mulder, C, Aldenberg, T, de Zwart, D, van Wijnen, JJ, Breure, AM (2005) Evaluating the impact of pollution on plant-Lepidoptera relationships. Environmetrics 16: 357373 CrossRef
Niehaus, M (1982) Technique for rearing the Small Tortoiseshell A. urticae without diapause at different temperatures (Lepidoptera: Nymphalidae). Entomol. Gen. 7: 365373
Niemi, GJ, McDonald, ME (2004) Application of ecological indicators. Annu. Rev. Ecol. Syst. 35: 89111 CrossRef
Pimentel D, Raven P (1999) Commentary: Increase in genetic engineering means less reliance on chemicals. St. Louis Post-Dispatch, 1 August 1999 B3
Pleasants, JM, Hellmich, RL, Dively, GP, Sears, MK, Stanley-Horn, DE, Mattila, HR, Foster, JE, Clark, PL, Jones, GD (2001) Corn pollen deposition on milk-weeds in or near cornfields. Proc. Natl. Acad. Sci USA 98: 1191911924 CrossRef
Poppy, G (2000) GM crops: environmental risks and non-target effects. Trends Plant Sci. 5: 46 CrossRef
Pullin AS (1987) Changes in leaf quality following clipping and regrowth of Urtica dioica, and consequences for a specialist insect herbivore, Aglais urticae. Oikis 49: 39–45 CrossRef
Ries, L, Debinski, DM (2001) Butterfly responses to habitat edges in the highly fragmented prairies of Central Iowa. J. Anim. Ecol. 70: 840852 CrossRef
Robinson, RA, Sutherland, WJ (2002) Post-war changes in arable farming and biodiversity in Great Britain. J. Appl. Ecol. 39: 157176 CrossRef
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: 117132 CrossRef
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: 219227 CrossRef
Sears, MK, Hellmich, RL, Stanley-Horn, DE, Oberhauser, KS, Pleasants, JM, Mattila, HR, Siegfried, BD, Dively, GP (2001) Impact of Bt corn pollen on monarch butterfly populations: a risk assessment. Proc. Natl. Acad. Sci USA 98: 1193711942 CrossRef
Shirai Y, Takahashi M (2005) Effects of transgenic Bt corn pollen on a non-target lycaenid butterfly Pseudozizeeria maha. Appl. Entomol. Zool. 40: 151–159
Stanley-Horn, DE, Dively, GP, Hellmich, RL, Mattila, HR, Sears, MK, Rose, R, Jesse, LCH, Losey, JF, Obrycki, JJ, Lewis, L (2001) Assessing the impact of Cry1Ab-expressing corn pollen on monarch butterfly larvae in field studies. Proc. Natl. Acad. Sci USA 98: 1193111936 CrossRef
Warren, MS (1997) Conserving Lepidoptera in a changing environment: a perspective from Western Europe. J. Insect Cons. 1: 14
Wirooks, L, Theissen, B (1998) Neue Erkenntnisse zur Nahrungsökologie und Phänologie von Makrolepidopterenraupen – Eine Zusammenfassung der Ergebnisse langjähriger Raupensuche unter besonderer Berücksichtigung ihrer Nahrungspflanzen und ihrer Phänologie. Melanargia 10: 69109
Wirooks, L, Theissen, B (1999) Neue Erkenntnisse zur Nahrungsökologie und Phänologie von Makrolepidopterenraupen – Eine Zusammenfassung der Ergebnisse langjähriger Raupensuche unter besonderer Berücksichtigung ihrer Nahrungspflanzen und ihrer Phänologie. Melanargia 11: 179, 147–224, 241–279
Woiwod, IP (1997) Detecting the effects of climate change on Lepidoptera. J. Insect Cons. 1: 149158 CrossRef
Wraight, CL, Zangerl, AR, Carroll, MJ, Berenbaum, MR (2000) Absence of toxicity of Bacillus thuringiensis pollen to black swallowtails under field conditions. Proc. Natl. Acad. Sci USA 98: 1190811912
Zabel, J, Tscharntke, T (1998) Does fragmentation of Urtica habitats affect phytophagous and predatory insects differentially? Oecologia 116: 419425 CrossRef
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. Natl. Acad. Sci USA 98: 1190811912 CrossRef