Environmental Science and Pollution Research

, Volume 18, Issue 1, pp 111–115

Status of feral oilseed rape in Europe: its minor role as a GM impurity and its potential as a reservoir of transgene persistence

  • Geoffrey R. Squire
  • Broder Breckling
  • Antje Dietz Pfeilstetter
  • Rikke B. Jorgensen
  • Jane Lecomte
  • Sandrine Pivard
  • Hauke Reuter
  • Mark W. Young
Short Research and Discussion Article

DOI: 10.1007/s11356-010-0376-1

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

Abstract

Purpose

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.

Methods

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.

Results

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.

Conclusions

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.

Keywords

Feral Oilseed rape Genetically modified GM coexistence Transgene persistence Cross pollination 

1 Introduction

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

The five studies (Table 1) in Tayside UK (region 1), Mid-Jutland Denmark (2), Bremen Germany (3), Braunschweig Germany (4) and Selommes France (5) were established independently in landscapes considered typical of agriculture within each region and range in area from 25 to >500 km2. The methodologies of survey by vehicle, covering roads, waysides, farm tracks and waste ground, backed up by inspection on foot of field margins and other features, and the recording of feral demographic data, have been described for four of the five areas (Charters et al. 1999; Dietz-Pfeilstetter et al. 2006; Menzel 2006; Pivard et al. 2008; Reuter et al. 2008). The methods in the Danish study area replicated those in the long established studies (1, 3). Here, a common analysis was applied to all five areas. The characteristics of each region and attributes of the feral populations were summarised (Table 1). All locational data were transferred to standard commercially available software packages for recording and processing geographic information, from which areas of fields and distances between feral locations and fields were estimated. The methods of recording demographic data (e.g. flowering plants, seed in each feral population) are given in the references cited above. Briefly, ferals were mapped as discrete groups of plants (studies 1 to 4) or, where they were in much higher density, as present or absent in segments along linear features (study 5). For each population in studies 1 to 4, numbers of flowering plants and numbers of plants with seed were estimated; this information was obtained from sub-samples in study 5. Numbers of seed per plant were usually measured on sub-samples in all studies. For comparison with plants and seed on crops, a range is given for each study area (e.g. 100–1,000) which encompassed the number of feral plants or seed measured or estimated over the years of study. Very large populations, which sometimes occurred in derelict fields or around road works, are not included in the analysis in Table 1.
Table 1

Characteristics of the study sites and feral populations and data derived to show the importance to coexistence

Number

Item

Tayside UK

Mid-Jutland /Bjerringbro Denmark

Bremen Germany

Braunschweig Germany

Selommes France

Characteristics of the study sites

1

Latitude

56.61

56.22

58.05

52.27

47.75

2

Longitude

−2.81

9.44

8.43

10.53

1.20

3

Area of survey (km−2)

515

25

570

140

42

4

Years of measurements

1993–1996

2005, 2006

2001, 2002, 2003, 2005

2001–2004

2003–2005

5

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

6

Area of arable land as % of total land area

53

75

50

46

90

7

Land area sown with oilseed rape (mean and range over years of study)

% Total land area, mean and range

4.7 (3.4–5.8)

5.1 (2.5–7.7)

2.5 (1.4–4.5)

3

14.7 (14.3–15.3)

% Arable land area, mean and range

8.8 (6.4–11.0)

6.7 (3.3–10.2)

5.0(2.8–9.0)

6

16.3 (15.9–17.0)

8

Season of sowing oilseed rape crop (%)

Spring

20

0

4

2

0

Autumn (winter)

80

100

96

98

100

Feral populations and implications for geneflow

9

Frequency of feral sites, mean and range among years (km−2)

0.37 (0.15–0.70)

0.70 (0.56–0.84)

1.4 (0.9–2.8)

0.21 (0.06–0.37)

15.4 (13.3–17.1)

10

Total feral plants flowering, estimated to be within range shown (plants km−2)

All populations

10–10,000

100–1,000

10–100

1–100

100–1,000

Population up to 100 plants

1–10

10–100

1–10

1–10

10–100

11

Feral sites flowering simultaneously with crop (%)

>90%

>95%

80%

Not measured

>90%

12

Feral seed (number seed km−2)

100–1,000

100–1,000

1,000–10,000

100–1,000

1,000–10,000

13

Feral plants as % Total oilseed rape

Flowering

<0.0002%

<0.0023%

<0.001%

<0.001%

<0.0002%

Seeding

<0.0001%

<0.00001%

<0.0001%

<0.00002%

<0.000001%

14

Evidence (visual) for persistence in same site for at least 3 years

Yes

Yes

Yes

Yes

Yes

15

Evidence (DNA or oil quality) for persistence of a type at a site for at least 3 years

Yes

Yes

Not tested

Yes

Yes

16

Evidence (DNA or oil quality) for seedbank at feral sites containing obsolete varieties

Yes

Yes

Not tested

Yes

Yes

17

% Feral populations within distance to nearest crop of oilseed rape in flower (all years combined)

10 m

10

19

5

Not measured

15

100 m

25

19

10

52

1 km

>75

90

80

99

2 km

>90

100

Not measured

100

18

Maximum % populations affected by weed management

45%

95%

60%

75%

25%

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.

3 Results

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.

4 Discussion

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.

Acknowledgements

The EU FP6 project SIGMEA funded this comparison of demographic studies.

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Geoffrey R. Squire
    • 1
  • Broder Breckling
    • 2
  • Antje Dietz Pfeilstetter
    • 3
  • Rikke B. Jorgensen
    • 4
  • Jane Lecomte
    • 5
    • 6
    • 7
  • Sandrine Pivard
    • 5
    • 6
    • 7
  • Hauke Reuter
    • 2
  • Mark W. Young
    • 1
  1. 1.SCRIDundeeUK
  2. 2.University of BremenBremenGermany
  3. 3.Julius Kühn-InstituteBraunschweigGermany
  4. 4.Riso National Laboratory for Sustainable EnergyTechnical University of DenmarkRoskildeDenmark
  5. 5.Laboratoire Ecologie Systématique et EvolutionUniversité Paris-Sud 11OrsayFrance
  6. 6.Laboratoire Ecologie Systématique et EvolutionCNRSOrsayFrance
  7. 7.Laboratoire Ecologie Systématique et EvolutionAgroParisTechParisFrance