Feral genetically modified herbicide tolerant oilseed rape from seed import spills: are concerns scientifically justified?

One of the concerns surrounding the import (for food and feed uses or processing) of genetically modified herbicide tolerant (GMHT) oilseed rape is that, through seed spillage, the herbicide tolerance (HT) trait will escape into agricultural or semi-natural habitats, causing environmental or economic problems. Based on these concerns, three EU countries have invoked national safeguard clauses to ban the marketing of specific GMHT oilseed rape events on their territory. However, the scientific basis for the environmental and economic concerns posed by feral GMHT oilseed rape resulting from seed import spills is debatable. While oilseed rape has characteristics such as secondary dormancy and small seed size that enable it to persist and be redistributed in the landscape, the presence of ferals is not in itself an environmental or economic problem. Crucially, feral oilseed rape has not become invasive outside cultivated and ruderal habitats, and HT traits are not likely to result in increased invasiveness. Feral GMHT oilseed rape has the potential to introduce HT traits to volunteer weeds in agricultural fields, but would only be amplified if the herbicides to which HT volunteers are tolerant were used routinely in the field. However, this worst-case scenario is most unlikely, as seed import spills are mostly confined to port areas. Economic concerns revolve around the potential for feral GMHT oilseed rape to contribute to GM admixtures in non-GM crops. Since feral plants derived from cultivation (as distinct from import) occur at too low a frequency to affect the coexistence threshold of 0.9% in the EU, it can be concluded that feral GMHT plants resulting from seed import spills will have little relevance as a potential source of pollen or seed for GM admixture. This paper concludes that feral oilseed rape in Europe should not be routinely managed, and certainly not in semi-natural habitats, as the benefits of such action would not outweigh the negative effects of management.

[1]  Wilhelm Claupein,et al.  Sleepers in the soil—Vertical distribution by tillage and long-term survival of oilseed rape seeds compared with plastic pellets , 2010 .

[2]  Philip J. Dale,et al.  Opportunities for gene transfer from transgenic oilseed rape (Brassica napus) to related species , 1994, Transgenic Research.

[3]  Christopher Preston,et al.  Canola (Brassica napus L.) seedbank declines rapidly in farmer-managed fields in South Australia , 2008 .

[4]  Nobuyoshi Nakajima,et al.  Monitoring the escape of transgenic oilseed rape around Japanese ports and roadsides. , 2005, Environmental biosafety research.

[5]  M. Crawley,et al.  Burial and seed survival in Brassica napus subsp. oleifera and Sinapis arvensis including a comparison of transgenic and non–transgenic lines of the crop , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[6]  Wilhelm Windhorst,et al.  An integrative methodology to predict dispersal of genetically modified genotypes in oilseed rape at landscape-level—A study for the region of Schleswig-Holstein, Germany , 2011 .

[7]  Paul Christou,et al.  EU legitimizes GM crop exclusion zones , 2011, Nature Biotechnology.

[8]  Michael J. Crawley,et al.  Seed limitation and the dynamics of feral oilseed rape on the M25 motorway , 1995, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[9]  D. Reheul,et al.  Ethics in the Societal Debate on Genetically Modified Organisms: A (Re)Quest for Sense and Sensibility , 2006 .

[10]  Roger W. Payne,et al.  Weed control in conventional and herbicide tolerant winter oilseed rape (Brassica napus) grown in rotations with winter cereals in the UK , 2008 .

[11]  Aurélie Garnier,et al.  Measuring and modelling anthropogenic secondary seed dispersal along roadverges for feral oilseed rape. , 2008 .

[12]  Clive James,et al.  Global status of commercialized biotech/GM crops: 2006. , 2006 .

[13]  Francisca López-Granados,et al.  Effect of environmental conditions on the dormancy and germination of volunteer oilseed rape seed (Brassica napus) , 1998, Weed Science.

[14]  S. Luijten,et al.  Baseline study of the distribution and morphology of Brassica napus L. and Brassica rapa L. in the Netherlands , 2010 .

[15]  B. Tinland,et al.  General Surveillance: Roles and Responsibilities The Industry View , 2007, Journal für Verbraucherschutz und Lebensmittelsicherheit.

[16]  D. Bartsch National safeguard clauses (Art. 23/ RL 2001/18) – The role of EFSA & National Biosafety Committees , 2009, Journal für Verbraucherschutz und Lebensmittelsicherheit.

[17]  Nobuyoshi Nakajima,et al.  Detection of feral transgenic oilseed rape with multiple-herbicide resistance in Japan. , 2006, Environmental biosafety research.

[18]  Christian Damgaard,et al.  Prediction of the combined effect of various GM contamination sources of seed: A case study of oilseed rape under Danish conditions , 2007 .

[19]  Inge Huybrechts,et al.  Competitiveness of transgenic oilseed rape , 1995, Transgenic Research.

[20]  Hails,et al.  Genetically modified plants - the debate continues. , 2000, Trends in ecology & evolution.

[21]  Rikke Bagger Jørgensen,et al.  The variability of processes involved in transgene dispersal—case studies from Brassica and related genera , 2009, Environmental science and pollution research international.

[22]  Alexandra Deville,et al.  Suivi de terrain, expérimentations et modélisation : des approches complémentaires pour l'étude de l'impact des populations de colza hors-champ sur les flux de gènes au sein des agro-écosystèmes , 2004 .

[23]  Sylvie Huet,et al.  Where do the feral oilseed rape populations come from? A large‐scale study of their possible origin in a farmland area , 2008 .

[24]  A. Dietz-Pfeilstetter,et al.  In-field frequencies and characteristics of oilseed rape with double herbicide resistance. , 2009, Environmental biosafety research.

[25]  R. FitzJohn,et al.  Diversity of brassica (brassicaceae) species naturalised in Canterbury, New Zealand , 2004 .

[26]  T. Christiansen,et al.  Comitology between Political Decision-Making and Technocratic Governance: Regulating GMOs in the European Union , 2009 .

[27]  Hugh J. Beckie,et al.  Simple to complex: Modelling crop pollen-mediated gene flow , 2008 .

[28]  Sašo Džeroski,et al.  Characterizing the presence of oilseed rape feral populations on field margins using machine learning , 2008 .

[29]  C. Johnstone,et al.  Microsatellite amplification in Brassica napus cultivars: Cultivar variability and relationship to a long-term feral population , 2004, Euphytica.

[30]  Rikke Bagger Jørgensen,et al.  Adventitious presence of other varieties in oilseed rape (Brassica napus) from seed banks and certified seed , 2007, Seed Science Research.

[31]  Vinitha Cardoza,et al.  Canola (Brassica napus L.). , 2006, Methods in molecular biology.

[32]  Hugh J. Beckie,et al.  Persistence of an oilseed rape transgene in the environment , 2010 .

[33]  Hugh J. Beckie,et al.  GENE FLOW IN COMMERCIAL FIELDS OF HERBICIDE‐RESISTANT CANOLA (BRASSICA NAPUS) , 2003 .

[34]  Rikke Bagger Ørgensen Oilseed Rape: Co‐existence and Gene Flow from Wild Species , 2007 .

[35]  A. Dietz-Pfeilstetter,et al.  Pollen-mediated intraspecific gene flow from herbicide resistant oilseed rape (Brassica napus L.) , 2007, Transgenic Research.

[36]  Alan Raybould,et al.  Tiered tests to assess the environmental risk of fitness changes in hybrids between transgenic crops and wild relatives: the example of virus resistant Brassica napus. , 2005, Environmental biosafety research.

[37]  Nobuyoshi Nakajima,et al.  Monitoring the occurrence of genetically modified oilseed rape growing along a Japanese roadside: 3-year observations. , 2009, Environmental biosafety research.

[38]  Matty Demont,et al.  Regulating coexistence of GM and non-GM crops without jeopardizing economic incentives. , 2008, Trends in biotechnology.

[39]  B. Tinland,et al.  General Surveillance for Import and Processing: the EuropaBio approach , 2009, Journal für Verbraucherschutz und Lebensmittelsicherheit.

[40]  C. Lavigne,et al.  Modelling and estimating pollen movement in oilseed rape (Brassica napus) at the landscape scale using genetic markers , 2006, Molecular ecology.

[41]  Saso Dzeroski,et al.  Sustainable introduction of GM crops into european agriculture: a summary report of the FP6 SIGMEA research project * , 2009 .

[42]  G. Ramsay,et al.  Temperature-dependent germination traits in oilseed rape associated with 5'-anchored simple sequence repeat PCR polymorphisms. , 2000, Journal of experimental botany.

[43]  G. Grabherr,et al.  Molecular differentiation of commercial varieties and feral populations of oilseed rape (Brassica napus L.) , 2010, BMC Evolutionary Biology.

[44]  R. Hails,et al.  Genes invading new populations: a risk assessment perspective. , 2005, Trends in ecology & evolution.

[45]  B. Breckling,et al.  Status of feral oilseed rape in Europe: its minor role as a GM impurity and its potential as a reservoir of transgene persistence , 2011, Environmental science and pollution research international.

[46]  Mark Tepfer,et al.  Fitness and beyond: preparing for the arrival of GM crops with ecologically important novel characters. , 2009, Environmental biosafety research.

[47]  Anne-Marie Chèvre,et al.  Crop-to-wild gene flow, introgression and possible fitness effects of transgenes. , 2003, Environmental biosafety research.

[48]  Lyle F. Friesen,et al.  EVIDENCE OF CONTAMINATION OF PEDIGREED CANOLA (BRASSICA NAPUS) SEEDLOTS IN WESTERN CANADA WITH GENETICALLY ENGINEERED HERBICIDE RESISTANCE TRAITS , 2003 .

[49]  Gerhard Embacher,et al.  Feral Oilseed Rape – Investigations on its Potential for Hybridisation Forschungsberichte der Sektion IV Band 3/2006 Feral Oilseed Rape – Investigations on its Potential for Hybridisation Forschungsberichte der Sektion IV , 2006 .

[50]  Wilhelm Claupein,et al.  Fecundity of volunteer oilseed rape and estimation of potential gene dispersal by a practice-related model , 2007 .

[51]  R. Jørgensen,et al.  Long-term persistence of GM oilseed rape in the seedbank , 2008, Biology Letters.

[52]  D. Bartsch,et al.  Implications for hybridization and introgression between oilseed rape (Brassica napus) and wild turnip (B. rapa) from an agricultural perspective. , 2004 .

[53]  Dirk Reheul,et al.  Quantifying the introgressive hybridisation propensity between transgenic oilseed rape and its wild/weedy relatives , 2009, Environmental monitoring and assessment.

[54]  Christian Damgaard,et al.  Competitive interactions and the effect of herbivory on Bt‐Brassica napus, Brassica rapa and Lolium perenne , 2009 .

[55]  Jeremy Sweet,et al.  Risk assessment of GM plants: avoiding gridlock? , 2003, Trends in plant science.

[56]  Steven J. Shirtliffe,et al.  Secondary seed dormancy prolongs persistence of volunteer canola in western Canada , 2003, Weed Science.

[57]  M. Crawley,et al.  Ecology of transgenic oilseed rape in natural habitats , 1993, Nature.

[58]  Christopher Preston,et al.  Pollen-Mediated Movement of Herbicide Resistance Between Commercial Canola Fields , 2002, Science.

[59]  I. Kowarik,et al.  Long‐Distance Dispersal of Plants by Vehicles as a Driver of Plant Invasions , 2007, Conservation biology : the journal of the Society for Conservation Biology.

[60]  H. V. Gelder The Netherlands , 2004, Constitutions of Europe (2 vols.).

[61]  E. Waltz GM crops: Battlefield , 2009, Nature.

[62]  Marie-Josée Simard,et al.  Fitness of double vs. single herbicide–resistant canola , 2005, Weed Science.

[63]  S. Warwick,et al.  Do escaped transgenes persist in nature? The case of an herbicide resistance transgene in a weedy Brassica rapa population , 2008, Molecular ecology.

[64]  Geoffrey R. Squire,et al.  Temperature and heterogeneity of emergence time in oilseed rape , 1999 .

[65]  Nathalie Colbach,et al.  Post-harvest gene escape and approaches for minimizing it , 2008 .

[66]  Marie-Josée Simard,et al.  A Framework for Postrelease Environmental Monitoring of Second-generation Crops with Novel Traits , 2010 .

[67]  Marie-Josée Simard,et al.  Environmental and agronomic consequences of herbicide-resistant (HR) canola in Canada. , 2004 .

[68]  Linda Hall,et al.  Pollen flow between herbicide-resistant Brassica napus is the cause of multiple-resistant B. napus volunteers1 , 2000, Weed Science.

[69]  Olivier Sanvido,et al.  Coexistence of genetically modified (GM) and non-GM crops in the European Union. A review , 2011, Agronomy for Sustainable Development.

[70]  S. Warwick,et al.  The Frequency and Persistence of Volunteer Canola (Brassica napus) in Québec Cropping Systems* , 2002, Weed Technology.

[71]  Martin Hermy,et al.  Motor vehicles as vectors of plant species from road verges in a suburban environment. , 2006 .

[72]  Christopher A. Gilligan,et al.  Which traits promote persistence of feral GM crops? Part 2: implications of metapopulation structure , 2005 .

[73]  N. L. Innes Global Status of Commercialized Biotech/GM Crops: 2005. ISAAA Briefs No. 34. By C. James. Ithaca, NY, USA: ISAAA (2005), pp. 46, US$50.00. ISBN 1-892456-38-9 , 2006, Experimental Agriculture.

[74]  P. J. W. Lutman,et al.  The long-term persistence of seeds of oilseed rape (Brassica napus) in arable fields , 2003, The Journal of Agricultural Science.

[75]  G. C. Tucker Raphanus raphanistrum L. , 2008 .

[76]  G. E. Fogg Sinapis Arvensis L. , 1950 .

[77]  Aurélie Garnier,et al.  Using a spatial and stage-structured invasion model to assess the spread of feral populations of transgenic oilseed rape , 2006 .

[78]  Alexander J. Stein,et al.  International trade and the global pipeline of new GM crops , 2010, Nature Biotechnology.

[79]  Richard G. FitzJohn,et al.  Hybridisation within Brassica and allied genera: evaluation of potential for transgene escape , 2007, Euphytica.

[80]  Rikke Bagger Jørgensen,et al.  Introgression between oilseed rape (Brassica napus L.) and its weedy relative B. rapa L. in a natural population , 2001, Genetic Resources and Crop Evolution.

[81]  N. Ellstrand,et al.  Dangerous Liaisons?: When Cultivated Plants Mate with Their Wild Relatives , 2003 .

[82]  J. Gressel,et al.  Crop ferality and volunteerism , 2005 .

[83]  Wilhelm Claupein,et al.  Seed persistence of oilseed rape (Brassica napus): variation in transgenic and conventionally bred cultivars , 2004, The Journal of Agricultural Science.

[84]  Broder Breckling,et al.  A review on Interspecific Gene Flow from Oilseed Rape to Wild Relatives , 2004 .

[85]  James H. Clarke,et al.  How valuable is glyphosate to UK agriculture and the environment , 2010 .

[86]  D. L. Thomas,et al.  Influence of Timing and Method of Harvest on Rapeseed Yield , 1991 .

[87]  Allison A. Snow,et al.  Costs of transgenic herbicide resistance introgressed from Brassica napus into weedy B. rapa , 1999 .

[88]  A. Messean,et al.  Persistence of oilseed rape (Brassica napus L.) outside of cultivated fields , 2001, Theoretical and Applied Genetics.

[89]  A. Chèvre,et al.  Interspecific hybrids between a transgenic rapeseed (Brassica napus) and related species: cytogenetical characterization and detection of the transgene. , 1993, Genome.

[90]  James W. McNicol,et al.  Modelling the persistence of volunteer oilseed rape (Brassica napus) , 2006 .

[91]  Genetically modified organisms (GMOs): The significance of gene flow through pollen transfer , 2002 .

[92]  A. M. Timmons,et al.  Problems of risk assessment with genetically modified oilseed rape. , 1995 .

[93]  S. Warwick,et al.  Gene Flow, Invasiveness, and Ecological Impact of Genetically Modified Crops , 2009, Annals of the New York Academy of Sciences.

[94]  C. Lavigne,et al.  High diversity of oilseed rape pollen clouds over an agro‐ecosystem indicates long‐distance dispersal , 2005, Molecular ecology.

[95]  Steven J. Shirtliffe,et al.  Secondary dormancy, temperature, and burial depth regulate seedbank dynamics in canola , 2004, Weed Science.

[96]  S. Warwick Hybridization between transgenic Brassica napus L. and its wild relatives : Brassica raps L., Raphanus raphanistrum L., Sinapis arvensis L., and Erucastrum gallicum (Willd.) , 2003 .

[97]  Moritz von der Lippe,et al.  Crop seed spillage along roads : a factor of uncertainty in the containment of GMO , 2007 .

[98]  Stéphane M McLachlan,et al.  Landscape-scale distribution and persistence of genetically modified oilseed rape (Brassica napus) in Manitoba, Canada , 2010, Environmental science and pollution research international.

[99]  D. M. Bruce,et al.  PM—Power and Machinery: Seed Loss when Cutting a Standing Crop of Oilseed Rape with Two Types of Combine Harvester Header , 2002 .

[100]  Peter Kareiva,et al.  Can we use experiments and models in predicting the invasiveness of genetically engineered organisms , 1996 .

[101]  Les Levidow,et al.  GM crops on trial: Technological development as a real-world experiment , 2007 .

[102]  Nobuyoshi Nakajima,et al.  Rapeseed species and environmental concerns related to loss of seeds of genetically modified oilseed rape in Japan , 2010, GM crops.

[103]  Claire Lavigne,et al.  Spatial scale of insect‐mediated pollen dispersal in oilseed rape in an open agricultural landscape , 2011 .

[104]  Hugh J. Beckie,et al.  Transgenic crops : new weed problems for Canada? , 1999 .

[105]  Gerhard Wenzel,et al.  Outcrossing frequencies and distribution of transgenic oilseed rape (Brassica napus L.) in the nearest neighbourhood , 2006 .

[106]  C. Sausse,et al.  Environmental and landscape effects on cross-pollination rates observed at long distance among French oilseed rape Brassica napus commercial fields , 2007 .

[107]  Nigel Maxted,et al.  Estimating the potential for ecological harm from gene flow to crop wild relatives , 2007 .

[108]  Kate Berry,et al.  Persistence of seeds from crops of conventional and herbicide tolerant oilseed rape (Brassica napus) , 2005, Proceedings of the Royal Society B: Biological Sciences.

[109]  J. Sweet,et al.  Introgression from Genetically Modified Plants into Wild Relatives , 2004 .

[110]  J. Londo,et al.  Glyphosate drift promotes changes in fitness and transgene gene flow in canola (Brassica napus) and hybrids. , 2010, Annals of botany.

[111]  Hugh J. Beckie,et al.  Multiple herbicide–resistant canola can be controlled by alternative herbicides , 2004 .

[112]  S. Warwick,et al.  Hybridization between transgenic Brassica napus L. and its wild relatives: Brassica rapa L., Raphanus raphanistrum L., Sinapis arvensis L., and Erucastrum gallicum (Willd.) O.E. Schulz , 2003, Theoretical and Applied Genetics.

[113]  M. Crawley,et al.  Spatially structured population dynamics in feral oilseed rape , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[114]  Christopher A. Gilligan,et al.  Which traits promote persistence of feral GM crops? Part 1:implications of environmental stochasticity , 2005 .

[115]  Lenka Justinova,et al.  The responses of crop - wild Brassica hybrids to simulated herbivory and interspecific competition: implications for transgene introgression. , 2006, Environmental biosafety research.

[116]  H. Kuiper,et al.  Request from the European Commission related to the safeguard clause invoked by Austria on oilseed rape MS8, RF3 and MS8xRF3 according to Article 23 of Directive 2001/18/EC 1 Scientific Opinion of the Panel on Genetically Modified Organisms , 2009 .

[117]  Aurélie Garnier,et al.  Stochastic modelling of feral plant populations with seed immigration and road verge management. , 2006 .

[118]  Hauke Reuter,et al.  Would genetically modified dwarfed oilseed rape (Brassica napus) increase feral survival , 2008 .

[119]  James M. Bullock,et al.  Predicting fitness changes in transgenic plants: testing a novel approach with pathogen resistant Brassicas , 2006 .

[120]  Niels Mejlgaard,et al.  The 2010 Eurobarometer on the life sciences , 2011, Nature Biotechnology.

[121]  Weijun Zhou,et al.  Variation in the development of secondary dormancy in oilseed rape genotypes under conditions of stress , 2002 .

[122]  Stephen J. Galsworthy,et al.  Human-mediated dispersal of seeds over long distances , 2009, Proceedings of the Royal Society B: Biological Sciences.

[123]  Paul Christou,et al.  Going to ridiculous lengths—European coexistence regulations for GM crops , 2010, Nature Biotechnology.

[124]  Steven J. Shirtliffe,et al.  Relative contribution of genotype, seed size and environment to secondary seed dormancy potential in Canadian spring oilseed rape (Brassica napus) , 2004 .

[125]  D. J. Perry,et al.  Adventitious presence of GMOs: Scientific overview for Canadian grains , 2006 .

[126]  Steven J. Shirtliffe,et al.  Harvest losses of canola (Brassica napus) cause large seedbank inputs , 2003, Weed Science.

[127]  D. M. Bruce,et al.  Genetic variation for pod shatter resistance among lines of oilseed rape developed from synthetic B. napus , 1998 .

[128]  M. A. Neale,et al.  Seed losses in commercial harvesting of oilseed rape , 1996 .

[129]  Olivier Sanvido,et al.  Coexistence in the EU—return of the moratorium on GM crops? , 2008, Nature Biotechnology.

[130]  Antoine Messéan,et al.  Occurrence of genetically modified oilseed rape seeds in the harvest of subsequent conventional oilseed rape over time , 2007 .

[131]  Mike J. May,et al.  Botanical and rotational implications of genetically modified herbicide tolerance in winter oilseed rape and sugar beet (BRIGHT Project)(H-GCA Project Report No. 353) , 2004 .

[132]  H. Siegismund,et al.  Progressive introgression between Brassica napus (oilseed rape) and B. rapa , 2003, Heredity.

[133]  Hauke Reuter,et al.  Hazard mitigation or mitigation hazard? , 2008, Environmental science and pollution research international.

[134]  Barbara Elling,et al.  Sources of genetic diversity in feral oilseed rape (Brassica napus) populations , 2009 .

[135]  Stéphane M. McLachlan,et al.  Gene Flow and Multiple Herbicide Resistance in Escaped Canola Populations , 2008, Weed Science.

[136]  Christoph Then,et al.  Testbiotech analysis of EFSA Guidance on the environmental risk assessment of genetically modified plants , 2010 .

[137]  Richard G. FitzJohn,et al.  Predicting weed distribution at the landscape scale: using naturalized Brassica as a model system , 2008 .

[138]  M. Crawley,et al.  Biotechnology: Transgenic crops in natural habitats , 2001, Nature.

[139]  Muthukumar V. Bagavathiannan,et al.  Crop ferality: Implications for novel trait confinement , 2008 .

[140]  Masaharu Kawata,et al.  Dispersal and persistence of genetically modified oilseed rape around Japanese harbors , 2009, Environmental science and pollution research international.

[141]  H. Beckie,et al.  Transgenic oilseed rape along transportation routes and port of Vancouver in western Canada. , 2006, Environmental biosafety research.