Status of feral oilseed rape in Europe: its minor role as a GM impurity and its potential as a reservoir of transgene persistence
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- Cite this article as:
- Squire, G.R., Breckling, B., Dietz Pfeilstetter, A. et al. Environ Sci Pollut Res (2011) 18: 111. doi:10.1007/s11356-010-0376-1
Feral oilseed rape has become widespread in Europe on waysides and waste ground. Its potential as a source of GM impurity in oilseed rape harvests is quantified, for the first time, by a consistent analysis applied over a wide range of study areas in Europe.
The maximum contribution of feral oilseed rape to impurities in harvested crops was estimated by combining data on feral abundance and crop yield from five established, demographic studies in agricultural habitats in Denmark, Germany (2), France and the UK, constituting over 1,500 ha of land and 16 site-years of observations. Persistence of feral populations over time was compared by visual and molecular methods.
Ferals had become established in all regions, forming populations 0.2 to 15 km−2. The seed they produced was always <0.0001% of the seed on crops of oilseed rape in each region. The contribution of ferals to impurity in crops through accidental harvest of seed and through cross-pollination would be an even smaller percentage. Feral oilseed rape nevertheless showed a widespread capacity to persist in all regions and retain traits from varieties no longer grown.
Feral oilseed rape is not a relevant source of macroscopic impurity at its present density in the landscape but provides opportunity for genetic recombination, stacking of transgenes and the evolution of genotypes that under strong selection pressure could increase and re-occupy fields to constitute an economic weed burden and impurity in future crops.
KeywordsFeral Oilseed rape Genetically modified GM coexistence Transgene persistence Cross pollination
The rapeseed crop has been grown for at least 1,000 years in Europe but never so widely and intensely as it has since the 1970s, when the crop has given rise to highly visible feral plants along waysides, field margins and waste ground (Pivard et al. 2008; Reuter et al. 2008). Feral oilseed rape has been proposed as a source of GM impurity in oilseed rape and a means by which genetic material from crops or imported oilseeds can persist outside fields and be reintroduced to subsequent oilseed rape crops (Elling et al. 2009; Kawata et al. 2009; Knispel and McLachlan 2009; Pessel et al. 2001; Reuter et al. 2008). Other sources of GM impurity in oilseed rape have been well quantified. That through cross-pollination between fields is typically 0.1% or less (Hüsken and Dietz-Pfeilstetter 2007) and that transmitted over time through volunteer weeds can range widely, from around 10% in some fields (Andersen et al. 2009) down to 0.01% or less (D’Hertefeldt et al. 2008) where specific measures are imposed to control volunteers, such as delaying post-harvest tillage until shed seeds have germinated and avoiding subsequent crops in which oilseed rape can emerge and re-seed.
The potential roles of cross-pollination, volunteers and ferals have been considered in feasibility studies of coexistence if GM oilseed rape was introduced as a commercial crop (Demont and Devos 2008; Devos et al. 2009; Messéan et al. 2009). However, the specific contributions of feral oilseed rape to impurity, both during a cropping season and subsequently through dispersal of seed from feral habitats into fields, has not been systematically quantified by common methods over representative European landscapes. Opinions on its role in the coexistence of GM and other crops in Europe are at best conjectural, therefore. Notably, if ferals were to comprise a substantial proportion of the oilseed rape in any region, they would need to be accounted for in any management strategies designed to facilitate coexistence. This paper combines five demographic studies in agricultural regions of Europe to compare the size of the flowering and seeding populations in ferals and crops and to assess the current and potential contribution of ferals to the transfer of GM traits to non-GM oilseed rape.
2 Materials and methods
Characteristics of the study sites and feral populations and data derived to show the importance to coexistence
Mid-Jutland /Bjerringbro Denmark
Characteristics of the study sites
Area of survey (km−2)
Years of measurements
2001, 2002, 2003, 2005
Main arable crops
Cereals, grass, oilseed rape, potato
Cereals, winter oilseed rape
Cereals, maize, winter oilseed rape
Cereals, sugar beet, oilseed rape
Cereals, maize, sunflower, pea, millet
Area of arable land as % of total land area
Land area sown with oilseed rape (mean and range over years of study)
% Total land area, mean and range
% Arable land area, mean and range
Season of sowing oilseed rape crop (%)
Feral populations and implications for geneflow
Frequency of feral sites, mean and range among years (km−2)
Total feral plants flowering, estimated to be within range shown (plants km−2)
Population up to 100 plants
Feral sites flowering simultaneously with crop (%)
Feral seed (number seed km−2)
Feral plants as % Total oilseed rape
Evidence (visual) for persistence in same site for at least 3 years
Evidence (DNA or oil quality) for persistence of a type at a site for at least 3 years
Evidence (DNA or oil quality) for seedbank at feral sites containing obsolete varieties
% Feral populations within distance to nearest crop of oilseed rape in flower (all years combined)
Maximum % populations affected by weed management
The number of plants in oilseed rape fields in each region was estimated by multiplying the within-crop density that is recommended or typical for a region, usually 50 to 100 m−2 (plants), by the area of the crop determined from the geographic information software, except at region 4, where the area of the crop was an approximation from maps. Agronomic and census data on mean yield and mean seed mass in each region were additionally used to derive the number of crop seed produced in a region. Where uncertainty or a range existed in the available data, the maximum estimates for feral and the minimum for crop seed were used. Persistence of feral plants at sites over time, observed over a minimum of three years at all sites, was assessed first by the circumstantial evidence that feral plants recurred at a site (Charters et al. 1999; Pivard et al. 2008). Evidence of persistence had also been examined (except region 3) at 10% or fewer sites using a variety of methods, including genetic markers that can distinguish individual varieties (Charters et al. 1996; Dietz-Pfeilstetter et al. 2006) and biochemical profiles that can distinguish broad groups of varieties (Pessel et al. 2001). Given that various methods were applied to different numbers of sites, the results were here standardised to provide qualitative answers to the questions of whether ferals had the capacity to persist over at least 3 years at a site and whether a feral site could contain varieties that were no longer grown in the region.
The percentage of agricultural land within the study area ranged from >90% at region 5 to around 50% at regions 1 and 3 where the area included forested and urban land. The percentage of the land area sown with oilseed rape was similar in the four northern regions, means ranging from 2.5% to 5.1%, but greater at 14.7% in the southernmost region 5. The number of locations at which feral plants were found (see Section 2) averaged over years within a region ranged from 0.21 to 1.4 km−2 among the northern regions but was greater at 15.5 km−2 at region 5. A location at which feral demographic data were estimated typically contained 1 to 100 flowering feral plants, but some contained more than 1,000. The number of seed set on feral plants was in the range 100 to 1,000 km−2 at regions 1, 2 and 4 and 1,000 to 10,000 km−2 at regions 3 and 5.
The regions differed less in number of feral plants or seeds when expressed per unit area of crop. The highest percentage of flowering ferals was around 0.002% (two flowering ferals for 100,000 crop plants) and the percentage of seed on ferals was in all cases <0.0001%, i.e., less than one feral seed for 1,000,000 crop seed (Table 1). This estimate for seed can also be taken as an absolute maximum for GM impurity arising through seed in the improbable event that all feral seed was harvested with the crop. The actual contribution to impurity by this means would be much less since 81% to 95% of feral plants were located more than 10 m from an oilseed rape field (Table 1). The contribution by flow of pollen from ferals to fields should also be small due to the steep reduction in the frequency of cross-fertilisation with distance (Hüsken and Dietz-Pfeilstetter 2007).
The demographic information from all five regions was consistent in showing feral populations can recur at a site for at least 3 years (the maximum recorded interval at every site). Recurrence over at least 4 years was observed in regions, 1, 3, 4 and 5. The maximum recurrence over 4 years was 16% of sites in region 5. Moreover, the demographic data were consistent in showing persistence in the seedbank allowed plants to recur after an absence of a year or more. Molecular and biochemical markers showed consistently among regions that feral sites can contain plants with the same varietal profile for at least 3 years and contain varieties last commercially grown three or more years previously, and in two instances at least eight (region 5) and 10 (region 1) years previously.
The systematic comparison of demographic information in these five, independent study areas enables definitive statements on the importance of feral oilseed rape to gene transfer between GM and non-GM crops in Europe, should GM oilseed rape be introduced commercially. Feral oilseed rape had become established throughout all five regions, but the maximum contribution of ferals to impurity in crops would be very much less than the contribution by cross pollination between fields and by volunteer weeds in fields and would by itself be at least four orders of magnitude below the current EC threshold of 0.9% for adventitious presence of GM seed (Messéan et al. 2009). While the estimates here assume an impurity based on regional collection of yield, as occurs in some parts of Europe, the situation is unlikely to be different for impurities assessed at the scale of the field or farm. The only contrary circumstances would be where very large numbers of ferals (>10,000 individuals) occur in derelict fields or building sites or where moderate to large populations occur adjacent to very small crop fields (e.g. a fraction of a hectare); but for the purpose of managing coexistence, such populations are readily observable and can be dealt with individually to avoid impurity.
The potential of GM ferals to introduce impurity after withdrawal of a GM crop would decline below the estimated maximum, provided the GM trait was selectively neutral. The potential for increase would remain great, however, since long-term persistence, even in low numbers, provides an opportunity for genetic recombination and stacking of traits that give, say, tolerance to herbicides or other stresses. Under strong selection pressure, for instance if herbicide-tolerant feral genotypes were treated with the respective herbicide, evolved genotypes could increase rapidly, re-colonise fields and thereby join existing volunteer populations to increase the economic weed burden and the potential for impurity.
The EU FP6 project SIGMEA funded this comparison of demographic studies.