The Institute of Health and Environmental Research Inc. (IHER)
is a not-for-profit research institute with a scientific interest
in the safety of genetically modified (GM) organisms,
particularly those destined for food.
Dr Phil Davies discusses the risks of GM genes in GM crops entering non-GM crops, insects and other organisms
This document appears as Chapter 4 in the book: Recoding Nature: Critical Perpectives on Genetic Engineering, edited by Richard Hindmarsh and Geoffrey Lawrence and published by the University of New South Wales Press in February 2004. The text of the chapter appears on pages 71 to 81 of the book, while the references appear on pages 226 to 228.
Dr Phil Davies
Davies P. Gene Flow and Genetically Engineered Crops. In: Hindmarsh R, Lawrence G, editors. Recoding Nature Critical Perspectives on Genetic Engineering. Sydney: UNSW Press; 2004. p. 71-81.
The cultivation of genetically engineered (GE) crops has attracted much controversy. People are concerned about effects of GE crops on human health and on the environment, following on from earlier harmful agricultural technologies, including insecticides, herbicides, nematicides, fungicides and mineral fertilisers. A key issue is the containment of GE crops and modified genes after they are released into the environment. Questions frequently raised include: Will GE crops become weeds difficult to control? Can engineered genes escape from the crop into weed species and create more aggressive weeds? Will engineered genes escape from the crop to pathogenic bacteria or viruses? Can GE crop products be separated from non-GE products to allow people the choice of eating non-GE products? Can the purity of non-GE crops be maintained to meet marketing requirements?
A responsible approach to regulating GE crops would ensure that such questions are rigorously addressed before the release of the GE crop into the environment. This, however, this has not been the case, and there is an increasing number of examples of genetic pollution - engineered genes contaminating crops, grain samples and foods.
In Canada, where GE canola has been grown for several years, there are clear examples of cross-pollination between neighbouring GE crops genetically modified for resistance to different herbicides, and non-GE crops. Progeny grown from the cross-pollinated seed are resistant to multiple herbicides. This has created problems for chemical control of plants containing multiple resistance.1 It has also created legal problems for a number of North American farmers who have been found to have GE canola growing on their properties without the required licensing agreements. In many cases, the GE canola is likely to have contaminated the farmers’ paddocks through windborne seed or pollen. However the courts have determined that it does not matter how the GE plants came to be there, the fact that they were growing without a licence agreement is enough to breach the genetic engineers’ intellectual property rights.2 These cases have been very costly to the farmers concerned. Similar problems are likely to follow in Australia with any commercial release of GE canola (see also Chapters 3 and 7).
In the United States, a GE variety of maize known as StarLink has been grown extensively. It was approved as an animal feed, but not for human consumption because of its potential to trigger allergic reactions. Despite attempts to segregate StarLink maize, there have been many reports of food-grade maize contaminated with StarLink grain.3 This genetic pollution has presented an unnecessary risk to human health. It has cost more than US $1 billion to test and recall contaminated products. Japan and the European Union have rejected many export shipments containing traces of the StarLink grain.
Traces of StarLink maize have also been detected in food products imported into the Australian food supply.4 Australia imported GE maize from the USA in December 2002 with the condition imposed by the Australian Gene Technology Regulator that it be used only as animal feed. In February 2003, it was reported that some of this GE maize had contaminated a silo of wheat awaiting export.5 Fortunately for the grain exporters, the contamination was detected early enough to remove the GE maize before loading the ship; detection by the importing countries may have led to rejection of the shipment on arrival.
The development of experimental GE crops for the production of pharmaceutical products also caused public concern when it was found that a soya bean crop grown in the United States had been contaminated with maize genetically engineered to produce a pig vaccine.6 The maize weeds found in the soya bean field grew from seed spilt during the previous season’s GE maize harvest. The contaminated crop was destroyed. This event also highlights the ease with which crops containing pharmaceuticals may contaminate food crops.
A longer-term consequence of genetic pollution is the contamination of traditional land race crop varieties, essential for maintaining the genetic diversity necessary for sustainable crop production and development of new crop varieties. Contamination of the traditional maize landraces in Mexico was first reported in November 2001.7 Following initial controversy about the validity of this report,8 further experiments have indicated that the contamination does exist, although explanations of how it came about are inconclusive.9 Although the consequences of contaminating the centres of crop genetic diversity with artificial genes cannot reliably be predicted, it is well recognised that these valuable gene pools should be preserved in their natural state (as Chapter 14 also highlights with regard to genetic erosion caused by the spread of monoculture crops).
Public concern about GE crops is now highly evident, and concern among scientists is gaining increasing exposure in a media environment not known for promoting open debate or diversity of opinion.10 It is essential that transparent and rigorous scientific and public evaluation of GE crops be undertaken to protect our natural heritage. To contribute to that evaluation, this chapter first discusses the role of plants in sustaining life, then gene dispersal through pollen, and finally the potential hazards of genetically engineered plants. With regard to the latter, I present seven hypotheses related to the proposition that, because of gene flow, GE crops will have significant effects on the environment and human health.
Plants are the foundation for life on earth. Through photosynthesis, they harness the sun’s energy to fuel the biochemical processes essential for the existence of the diversity of life around us. Driving the growth of animals, the flight of birds, the movement of fish through the oceans, is the energy that plants capture from the sun.
Although plants provide the energy for biological activity, they are dependent on other organisms for their long-term survival and propagation. Plants could not exist in the absence of the diverse array of organisms that form natural ecosystems. The flowering plants which cover the forests, plains and agricultural lands rely on myriad bacteria, fungi and insects to decompose dead organisms and mineralise the nutrients essential for plant growth. Because most terrestrial flowering plants are also sedentary, they must rely on insects, birds or animals to transport their seed or pollen to different places.
Pollen is a specialised phase of the plant life cycle which is essential for sexual reproduction. Also known as the male gametophyte, it is produced in flowering plants in floral organs called anthers. Pollen is genetically distinct from the plant it comes from because it has only half of the genetic information encoded in the parent plant. The female gametophyte, or egg cell, contained in ovaries at the base of the floral organ known as the stigma, also possesses half of the genetic information encoded in the parent plant. The primary function of pollen is to transport the plant’s genes to the flower of another plant, where it may fertilise the female gametophyte, creating a new seed containing the combined and complete genetic information from both plants.
Plants and most higher organisms contain duplicate sets of genetic information. These are similar, but not identical. One set of genes derives from the male parent and the other from the female parent. For example, for a single pollination event in wheat, the pollen parent may contribute genes encoding red seed, short plant height and poor baking quality and the female parent may contribute genes for white seed, tall height and good baking quality. The resulting seed containing both sets of genes will express characteristics, determined by the interaction of the genes. The gene for red seed may dominate the gene for white, resulting in red seed; the gene for shortness may mask the gene for tallness, producing a short plant; the genes for baking quality may interact resulting in intermediate baking quality. When this seed grows into a mature plant it will produce pollen (and eggs) with new combinations of the different genes. In this example, there will be eight possible combinations, such as red seed, short stems, poor quality; white seed, short stems, poor quality; red seed, long stems, poor quality, etc. In reality, each parent contributes thousands of different genes. This results in millions of possible gene combinations that create the vast array of genetic diversity observed within a particular plant species.
Pollen is carried from one plant to another either by animals, such as insects, birds and bats, or by the wind or water. Most cereal crop species and many tree species are wind pollinated, whereas many horticultural plants and pasture species are insect pollinated. Some insects, such as the honey bee, are pollinators of thousands of different plant species, whereas in other cases - for example, fig species pollinated by wasps - specific relationships have evolved between particular plant and insect species. 11 For the honey bee and many other species, pollen is also an important food source, providing protein and lipids not found in the nectar of the flowers they visit.
The complex relationship between plants and their insect pollinators has been evolving for 100 million years. Over the relatively short period of the past two decades, it has become possible to use recombinant DNA technology to overcome the natural boundaries of gene flow and introduce artificially constructed genes and genes from other organisms into plant species. Many of these GE crops are grown over large areas of North America and China.
Although much controversy has arisen about the potential impact of GE crops on natural ecosystems, agricultural ecosystems or human health, limited scientific thought or analysis has resulted. Proponents of GE crops frequently claim a scientific basis for their contention that GE crops will have zero or minimal environmental impact. The bases of these claims generally rely on the absence of empirical evidence for significant environmental impact. In other words, unless a GE crop can be shown unequivocally to be hazardous, it is assumed to be safe. This approach mirrors the current scientific method by which knowledge is advanced through the formulation and testing of hypotheses. A hypothesis – an explanation for a particular natural phenomenon – remains valid until evidence that disproves the hypothesis is found through observation or experiment.12 The formulation of hypotheses does not require logic, it may involve some guessing or intuition, and a hypothesis will remain valid until clearly disproved by empirical observation. In contrast, the testing of hypotheses does require logic and reasoning to either disprove the hypothesis or accept it as a reasonable explanation of the observed phenomenon. A good hypothesis leads to the discovery of new scientific insights.
The hypothesis that GE crops will have no significant environmental impact may be a good method for the advancement of scientific knowledge. However, as a tool for making decisions about whether GE crops should be released into the environment, it lacks the caution necessary for responsible, long-term environmental stewardship. A more cautious and responsible approach would be to adopt the hypothesis that GE crops will have a significant impact on the environment, and approve them for release only if a body of evidence accumulates to disprove this hypothesis (of relevance here is the precautionary principle, which is discussed in detail in Chapter 3).
The remainder of this chapter will discuss hypotheses related to the proposition that, because of gene flow, GE crops will have a significant effect on the environment and human health. The hypotheses are presented together with supporting evidence and discussion of the type of observations and experimental data required to disprove the hypotheses.
Pollen is the primary vector through which engineered genes may be transferred to non-transgenic crops. The distance travelled by pollen depends on the plant species and method of pollination. For short, self pollinated cereals such as wheat, barley, rice and oats, which are generally wind pollinated, the distances recorded for pollen dispersal are in the order of tens of metres or less.13 These distances are greater for taller outcrossing cereals such as maize and sorghum. The possible distance for cross-pollination is determined both by the physical distance that pollen can travel and the time for which pollen may remain viable. Cereal pollen is generally intolerant of desiccation, and therefore survives only a matter of hours after release from the anther into the atmosphere. However, if a GE cereal crop is growing in a paddock adjacent to a non-GE crop, it is highly likely that some GE pollen will pollinate the non-GE crop, resulting in GE seed contamination.
For crops that are insect pollinated, such as canola, sunflower, and many legume species, the opportunities for cross pollination between GE and non-GE crops are greater than for wind-pollinated species. Bees can carry pollen over distances in the order of five kilometres, so any non-GE crops within a five-kilometre radius of a GE insect pollinated crop such as canola risk being pollinated by GE pollen (see Chapter 7 for the concerns of organic farmers about this risk). There is evidence to support the hypothesis that GE crops will pollinate and contaminate non-GE crops.14 In North America, there have been several cases in which GE pollen has cross fertilised non-GE crops, resulting in GE seeds being harvested from a supposedly non-GE crop.15 In some cases, the farmer being prosecuted by the company that developed the GE crop for growing the crop without a license.
Because numerous examples exist where GE crops have cross pollinated with non-GE crops this hypothesis cannot be disproved and we must therefore accept the proposition that GE crops will pollinate and pollute non-GE crops. This does not mean that all GE crops will cause contamination in all cases, but it is a clear signal that a cautious approach is necessary.
In evolutionary terms, most crop species evolved recently. They developed larger and more palatable seeds and fruits than their wild relatives 5000 to 10 000 years ago with the development of agriculture and the repetitive selection of the largest and tastiest crops by the first farmers. Because crop species have only recently evolved, cross pollination is possible between many crops and their wild relatives, although the evolutionary distance between them often means that interspecific cross-pollination is less successful than cross pollination within the crop.
There is good evidence that GE crops will pollinate weed species to produce GE weeds. Experiments have shown that engineered genes from canola are transferred easily to the weedy relative Brassica campestris.16 Canola is also capable of cross pollinating with several other weed species including wild raddish (Raphanus raphanistrum) and buchan weed (Hirschfeldia incana) and can pollinate related crop species, including broccoli, cauliflower, cabbage and mustard.17 Other reports indicate that GE sunflower18 and GE sugar beet19 are capable of cross-pollinating with related weed species.
The hypothesis that GE crops will pollinate weed species to produce GE weeds is well supported with experimental data for many crop species. For some crops, the hypothesis may be disproved if it is demonstrated that related weed species do not exist in areas where the crop is grown.
Non-GE pollen is known to cause hay fever and allergies due to specific proteins expressed in the pollen.20 When new proteins are introduced into plants through genetic engineering, it is essential to test whether these proteins occur in pollen and to assess their allergenicity (see also Chapter 5). A protein naturally found in soil bacteria - for example some of the enzymes used to provide herbicide resistance to GE crops - may not normally affect humans, but if the same protein is found in pollen it may cause an allergic response.
GE proteins may also appear in foods which themselves are not genetically engineered. For example, pollen is an important component of honey, and if bee hives are located within 5 kilometres of a transgenic canola crop, or a weed which has inherited a GE protein through cross-pollination, the honey is likely to be contaminated with the GE protein. Keeping account of the spread of GE proteins is almost impossible.
One of the greatest concerns for human health is the development of molecular farming technology whereby crops are genetically engineered to produce pharmaceuticals, vaccines, enzymes, hormones or industrial oils or polymers. The products of many of these GE crops would have obvious detrimental consequences for human health if mistakenly consumed as food. For example, a banana genetically engineered to produce a vaccine may not be visibly distinguishable from a normal banana and, without extraordinary care, may end up in food markets; or a pharmaceutical produced in a canola crop may end up in a non-GE crop through cross pollination. It is very difficult to segregate agricultural commodities for food and non-food use, as the StarLink maize example discussed earlier demonstrates.
The hypothesis that GE crops will carry genes which adversely affect human health cannot be disproved if crops are genetically engineered to produce non-food products such as pharmaceuticals, which may have serious consequences if consumed at unspecified dosage. Although obtaining evidence to reject this hypothesis would not be simple, some GE crops have already been allowed to enter the human food chain without any publicly accessible or credible, scientific evaluation (see also Chapter 5).
A gene that has been frequently incorporated in genetically engineered crops - known as the Bt toxin - is derived from the bacterial species Bacillus thuringiensis. Bt toxins kill certain species of butterfly, moth, fly and beetle and they are put into crop species to protect them from insect attack. For example, Bt cotton is resistant to the cotton bollworm and Bt corn is resistant to the corn borer.
There is increasing evidence, however, that insects other than the crop pest are affected by the GE crop. It has been observed, for example, that lacewing larvae that feed on insects which have been raised on Bt maize have significantly greater mortality than when raised on conventional maize.21 It has also been observed that if monarch butterflies consume Bt maize pollen present on milkweed leaves, their mortality increases significantly.22 In different transgenic crops containing Bt genes, it is likely that other predatory and parasitic insects will be similarly affected.23
The hypothesis that GE crops will adversely affect insect populations has ample supporting evidence, particularly for the use of Bt genes. For GE crops in which Bt is not used, there has been little analysis of the effect of the crop on insect species.
The impact of the Bt toxin on insects, earthworms and other soil-inhabiting organisms is also of concern. Although the Bt toxin exists naturally in the environment in Bacillus thuringiensis, it was not present in such large quantities until the development of GE crops containing it. The long-term effect on soil microorganisms is unknown. Another concern is the impact of chemicals applied to crops engineered to be resistant to various herbicides. GE herbicide-resistant varieties sold as a package with proprietary herbicides encourage increased use of specific herbicides, whose effects on soil flora and fauna are unknown.
The hypothesis that GE crops will adversely affect soil organisms is very difficult to disprove, especially considering that many of the organisms living in the soil are so little studied that they have not yet been allocated scientific names.
Many examples exist of the detrimental impact of technology on the environment. In Australian agriculture, the use of many chemicals - including the chlorinated hydrocarbon pesticides - have been banned. When a chemical pollutant is no longer allowed to be used, its existing residues slowly disintegrate through physical and biological processes until eventually it exists in negligible quantities. On the other hand, when a genetically engineered organism is released into the environment, it has the capacity to reproduce and spread and may be impossible to recall. Many weed species are plants that have been introduced into a new environment where they have attained some selective advantage over the species that already exist there. If a GE plant has some selective advantage, it may become established as a weed. This is already being observed in agricultural systems, where GE crops with resistance to particular herbicides are becoming weeds in subsequent crops because they can no longer be controlled with particular herbicides In Canada, for example, Brassica napus (oil seed rape) crops have been found to contain volunteers that are resistant to three difference herbicides, namely glyphosate, imidazoline and glufosinate.24
Finding evidence to disprove the hypothesis that engineered genes released into the environment cannot be contained may involve experiments examining the prospects for cross-pollination to weedy species. However, there remains the potential for engineered genes to escape from the GE crop by other means, such as horizontal gene transfer.
The movement of genes between species outside of the normal reproductive process is referred to as horizontal gene transfer. One example of horizontal gene transfer in nature is the transfer of DNA from the HIV retrovirus into human DNA to cause disease. Another example is crown gall disease of stone fruits where the bacterium Agrobacterium tumefaciens transfers some of its DNA into the plant’s DNA, causing disease. Genetic engineering is an artificial form of horizontal gene transfer, by which genes may be transferred between species. There have been several examples of the transfer of genes from plants to fungi or bacteria. In one case, engineered genes introduced into Datura, Brassica, and Vicia species were shown to be transferred to the fungus Aspergillus niger25
No adequate means exist for testing the environmental impact of an engineered gene that finds its way into a species in which, in nature, its presence was not intended. For example, a Bt toxin gene may escape from a GE crop plant into a fungus that is the food source of a particular insect. What will be the effect on the insect and the ecosystem? With the escape of engineered genes, it will become virtually impossible to preserve forests and natural ecosystems in their natural state. This is because there will be no way of ensuring that the engineered genes keep out of these ecosystems.
Another potential hazard is the development of new strains of virus. Most GE crops contain a piece of DNA from the Cauliflower Mosaic Virus to control the functioning of the engineered gene. There is a risk that viruses that attack GE plants may combine their genes with the engineered gene to create viruses with new characteristics, such as increased virulence on the host or the ability to infect different species. 26
There is ample evidence to support the hypothesis that engineered genes can be transferred to non-plant species. Because there is uncertainty about gene escape to other organisms and further uncertainty about the behaviour of the modified gene in that organism, release of the GE crop to the environment cannot be considered prudent.
The seven hypotheses presented above assert that genetically engineered crops may be a hazard to the environment and to human health. GE crops may cross-pollinate with non-GE crops and cross-pollinate with related weed species. GE crops may carry genes that adversely affect human health either through allergenicity or through toxicity. GE crops may also adversely affect insect species or soil organisms, and the engineered genes may find their way into non-plant species, in which their behaviour and environmental consequences are unknown. Unlike chemical environmental pollutants, GE organisms are living, replicating entities and cannot be readily recalled once released to the environment.
Evidence to refute these hypotheses is either difficult to obtain, or does not exist. In the absence of clear scientific evidence, supporters of genetic engineering often argue that decisions concerning the release of GE crops should be based on risk-benefit analysis, where GE crops are approved for release if the perceived benefits outweigh the estimated risks. This approach is imprecise, as quantification of the risks involves a large degree of conjecture. In addition, this approach is inequitable, as the benefits are generally restricted to the organisations who have developed the technology, whereas the risks are borne by the entire human population and the environment.
A preferable approach to assessing the release of GE crops would incorporate the Precautionary Principle which states:
When an activity raises threats of harm to human health or the environment, precautionary measures should be taken even if some cause and effect relationships are not fully established scientifically. In this context, the proponent of an activity, rather than the public should bear the burden of proof. The process of applying the precautionary principle must be open, informed and democratic and must include potentially affected parties. It must also involve an examination of the full range of alternatives including no action. 27
In conclusion, unless the hypotheses presented above can be clearly disproved, any release of genetically engineered crops should not be permitted. To proceed otherwise would be to jeopardise human health and wellbeing, and endanger the ecosystems which sustain life on earth.
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12 Popper, K. 1963. Conjectures and Refutations: The Growth of Scientific Knowledge, Routledge & Kegan Paul, London.
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18 Faure, N., Serieys, H. & Berville, A. 2002. Potential gene flow from cultivated sunflower to volunteer, wild Helianthus species in Europe, Agriculture Ecosystems and Environment, 89: 183-90.
19 Lavigne, C., Klein, E. & Couvet, D. 2002. Using seed purity data to estimate an average pollen mediated gene flow from crops to wild relatives, Theoretical and Applied Genetics, 104: 139-45.
20 Petersdorf, R., Adams, R., Braunwald, E. Isselbacher, K., Martin, J. & Wilson, J. (eds.). 1983. Harrison’s Principles of Internal Medicine, Tenth edition, McGraw-Hill International, p. 376.
21 Hilbeck, A. 2001. Implications of transgenic, insecticidal plants for insect and plant biodiversity, Perspectives in Plant Ecology Evolution and Systematics, 4: 43-61.
22 Losey, J., Rayor, L. & Carter, M. 1999. Transgenic pollen harms monarch larvae, Nature, 399: 214; Hansen Jesse L. & ObryckI, J. 2000. Field deposition of Bt transgenic corn pollen: Lethal effects on the Monarch butterfly, Oecologia, 125: 241-48.
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27 Anonymous. 1998. The precautionary principle, Rachel’s Environment and Health Weekly, 19 February, 586; see also Chapter 3 of this volume for commentary concerning the precautionary principle.