Ecological risks from invasive transgenic insect-resistant maize
Modern maize (Zea mays L.) is highly domesticated, originating from human selection of teosinte more than 8,000 years ago (Galinat 1988). The extensive modification of maize from teosinte has rendered it unable to establish self-sustaining populations outside agriculture (Wallace and Brown 1988; Hoeft et al. 2000; OECD 2003). Maize does not establish self-sustaining feral populations for several reasons: it has poor seed dispersal because its seeds do not dehisce from the cob; it lacks seed dormancy, and therefore tends to germinate in the autumn, resulting in failure to overwinter in cold climates (Palaudelmàs et al. 2009); and it is a poor competitor with native perennial vegetation, which outcompetes it for light, nutrients and water (Olson and Sander 1988).
Because of its inability to form self-sustaining feral populations, cultivation of maize poses negligible ecological risk to uncultivated areas. Ecological risk assessments for cultivation of transgenic maize test the hypothesis that the event in question has not changed the crop phenotype in traits thought to control its invasiveness potential, through either intended or unintended effects of transformation. If this hypothesis is corroborated, the transgenic maize is no more likely than conventional maize to invade non-agricultural habitats, and may be deemed to pose negligible ecological risk outside cultivation via this mechanism. Corroboration would also further suggest that ecological and population genetic risks posed by hybridisation between transgenic insect-resistant maize and wild relatives are negligible (Hokanson et al. 2010).
For regulatory risk assessments, the hypothesis of no increased weediness potential in transgenic maize is tested routinely in agronomic field trials that allow comparison of the vegetative vigour, phenology, reproductive behaviour, and susceptibility to pests, diseases and abiotic stress of the transgenic maize with one or more suitable non-transgenic comparators (Horak et al. 2007); dormancy and germination may also be compared in laboratory studies (e.g., Raybould et al. 2010). Similarity in these characters between the transgenic and non-transgenic maize corroborates the hypothesis of no increased weediness potential, and thereby indicates that the transgenic maize will pose negligible ecological risk in non-agricultural habitats owing to its inability to spread to and establish in those areas.
The comparative approach to the assessment of ecological risks of feral transgenic maize is usually sufficient for regulatory decision-making; direct measurement of the invasiveness of transgenic maize is not usually required. The experiment reported here was a direct test of the ability of several transgenic insect-resistant maize events to form feral populations under Mexican environmental conditions. The study was not triggered by findings of potentially harmful differences in comparative studies, but by a request for additional testing of the hypothesis of negligible risk from invasive feral transgenic maize owing to high concern about potential adverse effects on maize genetic diversity in its centre of origin.
The results of the study corroborate the hypothesis that transgenic insect-resistance traits do not increase the invasiveness potential of maize relative to non-transgenic maize, either through the intended effects of the traits or through harmful unintended effects of transformation. As expected from comparisons of characters associated with invasiveness potential conducted in agronomic field trials and in laboratory studies, the presence of insect-resistance traits did not increase the RC values of the transgenic maize hybrids. We conclude that in the environment of south Texas and in similar environments in Mexico, transgenic insect-resistant maize plants would be no better at establishing populations in an unmanaged environment than would non-transgenic maize; thus, cultivation of these events would pose negligible risk to the environment.
Judging the sufficiency of data for risk assessment
Regulatory risk assessments test hypotheses that a proposed action will not lead to harmful effects that are specified in, or deduced from, laws, policies or regulations. For risks from cultivating transgenic crops, the hypotheses are of two kinds: the intended phenotypic change to the crop will have no harmful side-effects; and there are no potentially harmful unintended changes resulting from transformation. Such risk hypotheses can never be proved because it is always possible that a harmful effect will result despite extensive testing and corroboration of the hypotheses. It follows that the amount of testing of risk hypotheses required for regulatory decision-making is a matter of judgement, not of scientific analysis (Raybould 2011). Regulators must balance the costs of too much testing of activities that pose low risk with those of too little testing of activities that appear to pose low risk, but which further testing would have shown to pose high risk (Caley et al. 2006; Chapman et al. 1998).
Many of the tests carried out for regulatory risk assessments for the cultivation of transgenic crops are conducted because it was thought that transgenesis might produce harmful unintended effects more often than would other methods of plant breeding, such as hybridization and mutagenesis, used to introduce phenotypic variation. Numerous molecular studies [reviewed by Ricroch et al. (2011)], and many years’ experience of selecting and breeding transgenic crops (Bradford et al. 2005), have extensively tested and corroborated the hypothesis that harmful unintended effects are no more likely to arise from transgenesis than from other methods of plant breeding. It is argued, therefore, that molecular analyses that test for potentially harmful unintended effects of transgenesis should no longer be required routinely (Herman et al. 2011). Similarly, compositional analysis may not be required for transgenic crops with input traits (e.g., herbicide tolerance and insect resistance) conferred by the production of a single protein with a discrete mode of action, although compositional analysis may still be required for crops with output traits where the genetic modification is intended to change biochemical pathways (Herman et al. 2009). The argument is also relevant for invasiveness potential: transgenic crops per se are no more likely to become invasive than are non-transgenic crops with similar phenotypes introduced by other methods, and studies of the invasiveness potential of a transgenic crop should not be required unless there is reason to believe that the introduced traits will increase the invasiveness potential of the crop.
Hypotheses that the intended trait will not increase invasiveness potential of a crop can often be tested adequately without field studies that simulate dispersal of transgenic crop seed outside agriculture. If the crop does not form self-sustaining feral populations, knowledge of the factors that prevent establishment and persistence of the crop may be a sufficient test. Maize is unable to establish outside agriculture because of poor dispersal, lack of dormancy and competition from perennial plants (see above), not because insects prevent feral maize plants from establishing or reproducing; therefore, accumulated observations on maize dispersal and competitive ability could be considered a sufficient test of the hypothesis that transgenic insect-resistant maize will not be invasive and, if so, a field study such as described here would not be required.
Finally, although existing data may be used to test risk hypotheses and indicate negligible probabilities of harmful effects through invasiveness of transgenic crops, certain new studies may be conducted because they make risk communication easier or change the perception of risk more effectively than arguments based on existing knowledge. Sjöberg (2004) makes two relevant points: first, “interference with nature” is an important element in the perceived risks of transgenic crops; and secondly, the probabilities of harmful events (i.e., risks) may be “hard to understand, and are based on elaborate and debatable models and assumptions”. If transgenic crops are seen as interference with nature, and if comparative risk assessment using data from field trials seems elaborate and debatable, a single experiment that shows a transgenic crop being overwhelmed by natural vegetation may be attractive to risk managers and decision-makers, regardless of whether it is triggered by significant uncertainty about risk.
In summary, an experiment that simulated the dispersal of maize seed into non-agricultural land under environmental conditions found in parts of Mexico showed, as expected, that maize was unable to form self-sustaining feral populations, and that transgenic insect-resistance did not increase the invasiveness potential of maize. The experiment increases confidence that the invasiveness potential of transgenic maize is predictable from agronomic field trials that compare the phenotypes of transgenic and non-transgenic maize. While the results of the experiment were unsurprising, the experiment may be useful for communicating the negligible ecological risks from invasive transgenic insect-resistant maize in Mexico.