3. ESTABLISHMENT AND REPRODUCTIVE SUCCESS OF OILSEED RAPE ( BRASSICA
3.3 R ESULTS
3.4.2 Comparison of cultivated and weedy species
confirm that seed production per plant on some ruderal sites may be substantial and can exceed my findings (Dietz-Pfeilstetter et al. 2006, Menzel 2006).
agricultural seeds lost in transport and not for seeds produced under ruderal conditions.
However, my seed viability tests show that seeds collected from ruderal OSR and B. rapa almost show no reduction in seed viability compared to commercial seeds.
The cultivated species displayed high seed viability and low levels of dormancy. In addition, they clearly exhibited greater plant fitness, as the proportion of seedlings which grew into reproducing individuals was also significantly and greatly higher compared with the weedy species, with 41.1 and 83.4% for OSR and B. rapa, compared to 8.7% for B. nigra and 2.9%
for R. raphanistrum. While B. rapa even produced more seeds per plant than the weedy relatives, OSR produced at least equal amounts. In both weedy species most individuals developed poorly, and only few well-developed individuals produced large amounts of seeds.
This L-shaped distribution in seed reproductive output has previously been described for populations of R. raphanistrum (Stanton 1985). Furthermore, interspecific competition within the containers will have favoured fast-developing species. B. rapa was observed to be the first to flower in early May, followed by OSR (mid- to late May). R. raphanistrum and B. nigra flowered considerably later in early June and mid-July, respectively. B. nigra was at a particular disadvantage as the only species with a considerable emergence in spring 2008, while seedlings of all other species emerged almost exclusively in fall 2007. In addition, B. nigra has much smaller seeds and consequently smaller seedlings than the other species, which can be disadvantageous in a competitive environment (Stanton 1985). Larger seedlings are more resistant to environmental hazards, have more reserves and gain better access to resources (Leishman et al. 2000). Thus, the cultivated species may have largely depleted resources such as light and nutrients, resulting in a poor development of B. nigra and R. raphanistrum.
Other studies confirm superior establishment success of OSR over B. nigra in competition with grassland vegetation under field conditions (Walker et al. 2004) and a tendency for higher seed production by B. rapa vs. B. nigra in non-competitive greenhouse experiments (Feldheim & Conner 1996).
3.4.3 Implications for transgene escape
The superior performance of the cultivated species on low-quality ruderal substrates indicates a higher potential weediness for OSR and B. rapa than expected. In spite of low substrate quality and a stressful environment in terms of resource competition, the cultivated species were “weedier” than B. nigra and R. raphanistrum in some aspects which are typically attributed to successful weeds (Ammann et al. 2000): the capacity to germinate and produce
seeds in a wide range of environments, to produce a very large number of seeds under favourable conditions, as well as a rapid growth through the vegetative phase to flowering.
Given that both OSR and B. rapa successfully established on ruderal soils and showed a high reproductive capacity, hybridisation of these species, which is frequent and may lead to transgene introgression in agricultural settings (see 1.2.1), may well occur in feral populations.
While it has been demonstrated that some domestication traits, such as a dwarfing gene (Rose et al. 2009), can reduce fitness, my findings suggest that crop genes in general are not disadvantageous in non-agricultural environments. Studies with crop-wild hybrids mostly show lower fitness for the hybrid than for the wild parent (reviewed in Campbell 2007, Ellstrand 2003 and Hails & Morley 2005), including hybrids of OSR and wild relatives (but see Hauser et al. 2003). However, these studies are mostly restricted to early-generation hybrids whose fitness may be influenced by effects such as outbreeding depression and heterosis (Burke & Arnold 2001, Ellstrand 2003), which may over- or underestimate the probability of crop genes to persist within weed populations (Campbell 2007).
Some studies investigating the consequences of specific domestication traits indeed confirm that crop traits can be beneficial to plant fitness in stressful or non-crop environments, for example large size of seedlings and plants, rapid growth, early flowering and large flowering disk diameter in sunflowers (Baack et al. 2008, Mercer et al. 2007). In contrast, random crop alleles in crop-wild hybrids of OSR and weedy B. rapa only showed a positive effect in the absence of competition (Rose et al. 2009). In several cases, conventional crop genes managed to persist in weeds for several years under natural conditions (genes from OSR persisting in weedy B. rapa (Hansen et al. 2001), or genes from R. sativus persisting in R. raphanistrum (Snow et al. 2001)), giving further indications that crop genes do not generally confer a selective disadvantage (Campbell 2007). More significantly, an invasive hybrid line of R. sativus and R. raphanistrum has completely replaced the wild progenitor in California and apparently led to its local extinction (Hegde et al. 2006).
Similarly, my study indicates that R. raphanistrum and B. nigra could potentially benefit from crop traits conferred by OSR. One has to keep in mind, though, that my results are restricted to first-year successional stages in the absence of vertebrate and slug herbivory where competition by perennial plants was minimal. All three factors can heavily influence long-term survival of feral OSR populations (Crawley et al. 1993). While my results hint at a lower competitive ability of the weedy relatives, further research is needed on resistance to
herbivores or to fungal attack and other mortality factors. Another, possibly more important factor, is long-term survival in the seed bank, which does occur in OSR (Lutman et al. 2003) but at generally lower rates than those observed in weedy relatives (Hails et al. 1997, Lutman et al. 2002). It is an important characteristic of annual weeds and a factor for feral population persistence (Ammann et al. 2000, Cheam 1995, Gressel 2005). For a full assessment of OSR weediness, the benefits and drawbacks of high dormancy levels versus high reproductive output in the first year need to be assessed in the view of long-term establishment success (see 6.1.5).
In conclusion, my findings do not support the common assumption that crop traits would necessarily be disadvantageous in a wild environment, especially under stressful conditions, and that selection against crop alleles would prevent or reduce the introgression of transgenes into wild relatives (Squire et al. 2010, Stewart et al. 2003). My findings imply that ruderal environments may well facilitate uncontrolled spread of transgenes from OSR. Even though it is a cultivated plant, OSR has proven successful under suboptimal soil conditions, displayed the potential for self-sustained population increase and even outperformed weedy relatives.
Despite the fact that feral populations are mostly short-lived, their potential for weediness should thus not be overlooked or minimised, especially if further fitness advantages, such as herbicide resistance, are conferred through a transgene. Apart from the dangers this poses through uncontrolled transgene spread via feral OSR populations, it also raises concern regarding transgene spread via weedy or cultivated relatives, which does not seem to be limited by negative fitness effects of conventional domestication traits. Ruderal sites may thus serve as suitable refuges facilitating transgene escape. Given that an intensive monitoring of these sites is very time-consuming, transgene spread via these sites may go largely unnoticed.
References
Ammann, K., Jacot, Y. & Al Mazyad, P. A. (2000) Weediness in the light of new transgenic crops and their potential hybrids. Journal of Plant Diseases and Protection, Special Issue XVII, 19–29.
Aono, M., Wakiyama, S., Nagatsu, M., Nakajima, N., Tamaoki, M., Kubo, A. & Saji, H. (2006) Detection of feral transgenic oilseed rape with multiple-herbicide resistance in Japan.
Environmental Biosafety Research, 5, 77–87.
Baack, E. J., Sapir, Y., Chapman, M. A., Burke, J. M. & Rieseberg, L. H. (2008) Selection on domestication traits and quantitative trait loci in crop–wild sunflower hybrids. Molecular Ecology, 17, 666–677.
Bell, D. T. & Muller, C. H. (1973) Dominance of California Annual Grasslands by Brassica nigra.
American Midland Naturalist, 90, 277–299.
Bond, J. M., Mogg, R. J., Squire, G. R. & Johnstone, C. (2004) Microsatellite amplification in Brassica napus cultivars: Cultivar variability and relationship to a long-term feral population.
Euphytica, 139, 173–178.
Breckling, B. & Menzel, G. (2004) Self-organised pattern in oilseed rape distribution - An issue to be considered in risk analysis. Risk Hazard Damage. Specification of Criteria to Assess Environmental Impact of Genetically Modified Organisms (eds B. Breckling & R. Verhoeven), pp.
73–88, Bonn.
Brouwer, W. (1976) Handbuch des speziellen Pflanzenbaues Band II. Paul Parey Verlag, Berlin, Hamburg.
Burke, J. M. & Arnold, M. L. (2001) Genetics and the fitness of hybrids. Annual Review of Genetics, 35, 31–52.
Campbell, L. G. (2007) Rapid evolution in a crop-weed complex (Raphanus spp.). Dissertation, Ohio State University, Ohio.
Champolivier, L. & Merrien, A. (1996) Effects of water stress applied at different growth stages to Brassica napus L. var. oleifera on yield, yield components and seed quality. European Journal of Agronomy, 5, 153–160.
Cheam, A. H. (1984) Coat imposed dormancy controlling germination in wild radish and fiddle dock seeds. Seventh Australian Weeds Conference, Perth, Western Australia.
Cheam, A. H. (1986) Seed production and seed dormancy in wild radish (Raphanus raphanistrum L.) and some possibilities for improving control. Weed Research, 26, 405–413.
Cheam, A. H. (1995) The Biology of Australian Weeds. 24. Raphanus raphanistrum. Plant Protection Quarterly, 10, 2–13.
Clarke, J. M. & Simpson, G. M. (1978) Influence of irrigation and seeding rates on yield and yield components of Brassica napus cv. Tower. Canadian Journal of Plant Science, 58, 731–737.
Claußen, G. (2007) Wildackersaaten für Feld und Wald. Wildackerfibel. Wolmersdorf.
Cramer, N. (1990) Raps. Züchtung - Anbau und Vermarktung von Körnerraps. Ulmer, Stuttgart.
Crawley, M. J. & Brown, S. L. (1995) Seed Limitation and the Dynamics of Feral Oilseed Rape on the M25 Motorway. Proceedings of the Royal Society of London B, 259, 49–54.
Crawley, M. J. & Brown, S. L. (2004) Spatially structured population dynamics in feral oilseed rape.
Proceedings of the Royal Society of London B, 271, 1909–1916.
Crawley, M. J., Hails, R. S., Rees, M., Kohn, D. & Buxton, J. (1993) Ecology of transgenic oilseed rape in natural habitats. Nature, 363, 620–623.
Diepenbrock, W. (2000) Yield analysis of winter oilseed rape (Brassica napus L.): a review. Field Crops Research, 67, 35–49.
Dietz-Pfeilstetter, A., Metge, K., Schönfeld, J. & Zwerger, P. (2006) Abschätzung der Ausbreitung von Transgenen aus Raps durch populationsdynamische und molekularbiologische Untersuchungen an Ruderalraps. Journal of Plant Diseases and Protection, Special Issue XX, 39–47.
Duffy, G., Grégoire, S. & Martinelli, A. (2007) Validation of Tetrazolium method for Brassica spp.
ISTA Method Validation Reports, 4. The International Seed Testing Association (ISTA), Bassersdorf.
DWD, Deutscher Wetterdienst (2010). http://www.dwd.de/ (12.09.2010).
Elling, B., Neuffer, B. & Bleeker, W. (2009) Sources of genetic diversity in feral oilseed rape (Brassica napus) populations. Basic and Applied Ecology, 10, 544–553.
Ellstrand, N. C. (2001) When Transgenes Wander, Should We Worry? Plant Physiology and Biochemistry, 125, 1543–1545.
Ellstrand, N. C. (2003) Dangerous liaisons? When cultivated plants mate with their wild relatives.
Johns Hopkins University Press, Baltimore, Maryland.
Ellstrand, N. C., Prentice, H.C. & Hancock, J.F. (1999) Gen Flow and Introgression from Domesticated Plants into their Wild Relatives. Annual Review of Ecology and Systematics, 30, 539–563.
Feldheim, K. & Conner, J. K. (1996) The Effects of Increased UV-B Radiation on Growth, Pollination Success, and Lifetime Female Fitness in Two Brassica Species. Oecologia, 106, 284–297.
Geisler, G. & Stoy, A. (1987) Untersuchungen zum Einfluß der Bestandesdichte auf das Ertragspotential von Rapspflanzen (Brassica napus L. var. napus). Journal of Agronomy and Crop Science, 159, 232–240.
Gressel, J. (2005) Crop Ferality and Volunteerism. Taylor & Francis Group, Boca Raton, Flrorida.
Gruber, S., Pekrun, C. & Claupein, W. (2004) Seed persistence of oilseed rape (Brassica napus):
variation in transgenic and conventionally bred cultivars. The Journal of Agricultural Science, 142, 29–40.
Hails, R. S. (2000) Genetically modified plants - the debate continues. Trends in Ecology & Evolution, 15, 14–18.
Hails, R. S. & Morley, K. (2005) Genes invading new populations: a risk assessment perspective.
Trends in Ecology & Evolution, 20, 245–252.
Hails, R. S., Rees, M., Kohn, D. D. & Crawley, M. J. (1997) Burial and seed survival in Brassica napus subsp. oleifera and Sinapis arvensis including a comparison of transgenic and non-transgenic lines of the crop. Proceedings of the Royal Society of London, 264, 1–7.
Hansen, L. B., Siegismund, H. R. & Jørgensen, R. B. (2001) Introgression between oilseed rape (Brassica napus L.) and its weedy relative B. rapa L. in a natural population. Genetic Resources and Crop Evolution, 48, 621–627.
Hauser, T. P., Damgaard, C. & Jørgensen, R. B. (2003) Frequency-Dependent Fitness of Hybrids between Oilseed Rape (Brassica napus) and Weedy B. rapa (Brassicaceae). American Journal of Botany, 90, 571–578.
Hegde, S. G., Nason, J. D., Clegg, J. M. & Ellstrand, N. C. (2006) The Evolution of California's Wild Radish Has Resulted in the Extinction of Its Progenitors. Evolution, 60, 1187–1197.
Holm, L. G., Plucknett, D. L., Pancho, J. V. & Herberger, J. P. (1977) The World's Worst Weeds.
Distribution and Biology. The University Press of Hawaii, Honolulu, Hawaii.
Holzner, W. & Numata, M. (1982) Biology and ecology of weeds. Geobotany, 2. Junk Publishers, The Hague.
Kivilaan, A. & Bandurski, R. S. (1973) The Ninety-Year Period for Dr. Beal's Seed Viability Experiment. American Journal of Botany, 60, 140–145.
Koehler, H. & Müller, J. (2003) Entwicklung der Biodiversität während einer 20 jährigen Sukzession als Grundlage für Managementmaßnahmen. Abschlussbericht FKZ 01 LC 0005, Universität Bremen, Bremen.
Leach, J. E., Stevenson, H. J., Rainbow, A. J. & Mullen, L. A. (1999) Effects of high plant populations on the growth and yield of winter oilseed rape (Brassica napus). The Journal of Agricultural Science, 132, 173–180.
Leishman, M. R., Wright, I. J., Moles, A. T. & Westoby, M. (2000) The evolutionary ecology of seed size. Seeds. The ecology of regeneration in plant communities (ed M. Fenner), pp. 31–58. CABI Publishing, Wallingford, New York.
Luijten, S. & de Jong, T. (2010) A baseline study of the distribution and morphology of Brasscica napus L. and Brassica rapa L. in the Netherlands. COGEM Report: CGM 2010-3, Leiden University, Leiden.
Lutman, P. J. W., Cussans, G. W., Wright, K. J., Wilson, B. J., Wright, G. M. & Lawson, H. M.
(2002) The persistence of seeds of 16 weed species over six years in two arable fields. Weed Research, 42, 231–241.
Lutman, P. J. W., Freeman, S. E. & Pekrun, C. (2003) The long-term persistence of seeds of oilseed rape (Brassica napus) in arable fields. The Journal of Agricultural Science, 141, 231–240.
Mekenian, M. R. & Willemsen, R. W. (1975) Germination Characteristics of Raphanus raphanistrum.
I. Laboratory Studies. Bulletin of the Torrey Botanical Club, 102, 243–252.
Mendham, N. J., Shipway, P. A. & Scott, R. K. (1981) The effects of delayed sowing and weather on growth, development and yield of winter oil-seed rape (Brassica napus). The Journal of Agricultural Science, 96, 389–416.
Menzel, G. (2006) Verbreitungsdynamik und Auskreuzungspotenzial von Brassica napus L. (Raps) im Goßraum Bremen. Basiserhebung zum Monitoring von Umweltwirkungen transgener Kulturpflanzen. Dissertation, University of Bremen, GCA-Verlag, Waabs.
Mercer, K. L., Andow, D. A., Wyse, D. L. & Shaw, R. G. (2007) Stress and domestication traits increase the relative fitness of crop–wild hybrids in sunflower. Ecology Letters, 10, 383–393.
Miller, P. R., Angadi, S. V., Androsoff, G. L., McConkey, B. G., McDonald, C. L., Brandt, S. A., Cutforth, H. W., Entz, M. H. & Volkmar, K. M. (2003) Comparing Brassica oilseed crop productivity under contrasting N fertility regimes in the semiarid northern Great Plains. Canadian Journal of Plant Science, 83, 489–497.
OECD Organisation for Economic Co-operation and Development (1997) Consensus Document on the Biology of Brassica napus L. (Oilseed Rape). http://www.oecd.org/science/biotrack/
27531440.pdf (16.07.13).
Parker, I. M. & Kareiva, P. (1996) Assessing the risks of invasion for genetically engineered plants:
Acceptable evidence and reasonable doubt. Invasion Biology. Biological Conservation, 78, 193–
203.
Pessel, F. D., Lecomte, J., Emeriau, V., Krouti, M., Messean, A. & Gouyon, P. H. (2001) Persistence of oilseed rape (Brassica napus L.) outside of cultivated fields. Theoretical and Applied Genetics, 102, 841–846.
Pilson, D. & Prendeville, H. R. (2004) Ecological Effects of Transgenic Crops and the Escape of Transgenes into Wild Populations. Annual Review of Ecology, Evolution and Systematics, 35, 149–
174.
Quinn, G. P. & Keough, M. J. (2007) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge.
Rapool Ring GmbH (2007) Spätsaat. http://www.rapool.de/printview.cfm/id/312/print/yes.html (30.11.2007).
Rathke, G. W., Christen, O. & Diepenbrock, W. (2005) Effects of nitrogen source and rate on productivity and quality of winter oilseed rape (Brassica napus L.) grown in different crop rotations. Field Crops Research, 94, 103–113.
Reeves, T. G. & Code, G. R. P. C. M. (1981) Seed production and longevity, seasonal emergence, and phenology of wild radish, (Raphanus raphanistrum L.). Australian Journal of Experimental Agriculture, 21, 524–530.
Rich, T. C. G. (1991) Crucifers of Great Britain and Ireland. Botanical Society of the British Isles, London.
Rieger, M. A., Potter, T. D., Preston, C. & Powles, S. B. (2001) Hybridisation between Brassica napus L. and Raphanus raphanistrum L. under agronomic field conditions. Theoretical and Applied Genetics, 103, 555–560.
Roberts, H. A. (1986) Seed Persistence in Soil and Seasonal Emergence in Plant Species from Different Habitats. Journal of Applied Ecology, 23, 639–656.
Roberts, H. A. & Boddrell, J. E. (1983) Seed survival and periodicity of seedling emergence in eight species of Cruciferae. Annals of Applied Biology, 103, 301–309.
Rose, C., Millwood, R., Moon, H., Rao, M., Halfhill, M., Raymer, P., Warwick, S., Al-Ahmad, H., Gressel, J. & Stewart, C. N. (2009) Genetic load and transgenic mitigating genes in transgenic Brassica rapa (field mustard) x Brassica napus (oilseed rape) hybrid populations. BMC Biotechnology, 9, 93.
Schafer, M. G., Ross, A. A., Londo, J. P., Burdick, C. A., Lee, E. H., Travers, S. E., van de Water, P.
K. & Sagers, C. L. (2011) The Establishment of Genetically Engineered Canola Populations in the U.S. PLoS ONE, 6, e25736.
Scheffler, J. A. & Dale, P. J. (1994) Opportunities for gene transfer from transgenic oilseed rape (Brassica napus) to related species. Transgenic Research, 3, 263–278.
Schlink, S. (1994) Ökologie der Keimung und Dormanz von Körnerraps (Brassica napus L.) und ihre Bedeutung für eine Überdauerung der Samen im Boden. Dissertation, University of Göttingen, Cramer, Berlin.
Schoenenberger, N. & D'Andrea, L. (2012) Surveying the Occurrence of subspontaneous glyphosate-tolerant genetically engineered Brassica napus L. (Brassicaceae) along Swiss railways.
Environmental Sciences Europe, 24, 23.
Schulz, K. & Troll, H. J. Beobachtungen über Winterfestigkeit und Spätsaatverträglichkeit von Winterraps, Winterrübsen und ihren Bastarden. Zeitschrift für Acker- und Pflanzenbau, 1959, 430–
441.
Sieling, K. & Christen, O. (1997) Effect of preceding crop combination and N fertilization on yield of six oil-seed rape cultivars (Brassica napus L.). European Journal of Agronomy, 7, 301–306.
Snow, A. A. & Morán Palma, P. (1997) Commercialization of Transgenic Plants: Potential Ecological Risks. BioScience, 47, 86–96.
Snow, A. A., Uthus, K. L. & Culley, T. M. (2001) Fitness of hybrids between weedy and cultivated radish: implications for weed evolution. Ecological Applications, 11, 934–943.
Sokal, R. & Rohlf, J. (1969) Biometry. The principles and practice of statistics in biological research.
W.H. Freeman and Company, New York.
Squire, G., Breckling, B., Dietz Pfeilstetter, A., Jørgensen, R. B., Lecomte, J., Pivard, S., Reuter, H. &
Young, M. (2010) Status of feral oilseed rape in Europe: its minor role as a GM impurity and its potential as a reservoir of transgene persistence. Environmental Science and Pollution Research, 18, 111–115.
Stanton, M. L. (1984) Seed Variation in Wild Radish: Effect of Seed Size on Components of Seedling and Adult Fitness. Ecology, 65, 1105–1112.
Stanton, M. L. (1985) Seed size and emergence time within a stand of wild radish (Raphanus raphanistrum L.): the establishment of a fitness hierarchy. Oecologia, 67, 524–531.
Stewart, C. N., Halfhill, M. D. & Warwick, S. I. (2003) Transgene introgression from genetically modified crops to their wild relatives. Nature Reviews Genetics, 4, 806–817.
Thompson, K. & Grime, J. P. (1983) A Comparative Study of Germination Responses to Diurnally-Fluctuating Temperatures. Journal of Applied Ecology, 20, 141–156.
Toole, E. (1946) Final Results of the Duvel Buried Seed Experiment. Journal of Agricultural Research, 72, 201–210.
TransGen (2013) Gentechnisch veränderter Raps - Anbauflächen weltweit.
http://www.transgen.de/anbau/flaechen_international/199.doku.html (06.11.2013).
Virtue, J. & Thomas, P. (1999) Field screening techniques to assess new crop weeds. 12th Australian Weeds Conference, Hobart, Australia.
Walker, R. L., Booth, E. J., Whytock, G. P. & Walker, K. C. (2004) Volunteer potential of genetically modified oilseed rape with altered fatty acid content. Agriculture, Ecosystems & Environment, 104, 653–661.
Warwick, S. & Francis, A. (2005) The Biology of Canadian weeds. 132. Raphanus raphanistrum, L.
Canadian Journal of Plant Science, 85, 709–733.
Warwick, S. I., Légère, A., Simard, M. J. & James, T. (2008) Do escaped transgenes persist in nature?
The case of an herbicide resistance transgene in a weedy Brassica rapa population. Molecular Ecology, 17, 1387–1395.
White, V. A. & Holt, J. S. (2005) Competition of Artichoke Thistle (Cynara cardunculus) with Native and Exotic Grassland Species. Weed Science, 53, 826–833.
Zijlstra, W. (2004) Comparing the Student's t and the ANOVA contrast procedure with five alternative procedures. Master thesis, Rijksuniversiteit Groningen, Groningen.