Agronomy Journal 92:797-803 (2000)
© 2000 American Society of Agronomy
FORUM
Genetically Modified Crops and the Environment
Joanne E. Bartona and
Miles Dracupb
a Centre for Legumes in Mediterranean Agriculture, Univ. of Western Australia, Nedlands, Western Australia 6907
b Agriculture Western Australia, Locked Bag 4, Bentley 6983 Australia
mdracup{at}agric.wa.gov.au
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ABSTRACT
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Genetic modification (GM) of crops provides new crop management options (production traits) and crops with industrial, pharmaceutical, and neutraceutical applications are likely to follow. The environmental benefits and risks of growing GM crops have drawn considerable, often polarized debate. This review seeks a balanced appraisal of environmental issues, and looks at principles associated with several GM production traits. Environmental assessment needs to consider the nature of the introduced trait, in the context of the biology of the plant and the environment it will be grown in (e.g., prospects of gene flow into other species). Interactions with the target ecosystem, including the possibility of cummulative impacts from organisms already released into the ecosystem (e.g., prospects for gene pyramiding) need to also be included in assessments. Current agricultural management practices and ecosystems have their own impacts on the environment, and it is against this background that the benefits and risks of releasing GM organisms should be judged. Before release, data collection on impacts of GMOs is temporally and spatially constrained, so caution must be exercised in decision making. Potential impacts also need to be monitored after release and the post-release monitoring framework needs scope to identify unforeseen impacts. The environmental sustainability of using GMOs will depend largely on wise management practices and monitoring must provide appropriate data to support continuing adaptation of management and regulation of GMOs.
Abbreviations: GM, genetic modification or genetically modified
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INTRODUCTION
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THE use of molecular biological techniques to manipulate DNA and thus alter the make-up of organisms has provided alternative strategies for on-farm management of weeds, pests, and disease (James, 1998). There is also the opportunity to grow crops with industrial, neutraceutical (functional foods), and pharmaceutical (medical compounds) applications. Environmental benefits and risks of GM plants have been debated at length (Brill, 1985; Colwell et al., 1985; Boulter, 1993; Harlander, 1990; Hileman, 1995; Lewis and Palevitz, 1999; Miflin, 1999; Nottingham, 1998; Porter, 1999; Raybould et al., 1999). Nevertheless, adoption of GM crops by the farming community has been rapid. More than 24 million ha of genetically modified (GM) crops were grown in the 1998 season (James, 1998) and about 40 million ha in the 1999 season (ERS, 1999). Continuing environmental concerns challenge further implementation of the technology in a debate that has become polarized and politicized (Glickman, 1999; Serageldin, 1999). It is argued that GM crops place the environment and human health at risk (Greenpeace, 1999; Natural Law Party, 1999) and that life sciences companies responsible for their introduction threaten global food security (Rural Advancement Foundation Int., 1999). The effects of GM corn pollen on larval development of the monarch butterfly (Losey et al., 1999) and the premature release of feeding trial data during GM product development have generated negative public opinion often associated with press coverage of technological controversy (Gaskell et al., 1999; Royal Society, 1999). Suspicion of the intentions of corporate players (Vidal, 1999) has been exacerbated by the provision of inaccurate information to regulators (Coghlan, 1999; Woolf, 1999) and proposals to control seed viability (Oliver et al., 1998). It is in this atmosphere of confrontation and distrust that the impact of GM plants on the environment is discussed. While there is a need to scientifically asses the environmental benefits resulting from the introduction of GM crops it is recognized that these will continue to be realized only if the international community is comfortable with the technology. Independent and transparent regulation, environmental impact assessment, and sensitivity to the political and human dimension of the debate are important. Key issues discussed in this paper include:- Does the technology generate organisms with the potential to interact differently with the environment?
- Can risks and benefits associated with these interactions be assessed?
- Are there environmental benefits from the technology?
- Are there risks to the environment from the technology and can these be managed?
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Does the Technology Generate Organisms with the Potential to Interact Differently with the Environment?
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Successful production of GM crops has resulted in the introduction of a range of traits to farming systems. The novel mechanisms involved in GM crop production and the possible effects of marker genes and specific traits in GM crops on human health are discussed in other papers (Kaeppler, 2000). Whether the traits introduced into GM crops are output traits (value enhancing traits for end users, e.g., high methionine protein seed production in lupins) or input traits (agronomic traits, e.g., herbicide tolerance), they carry additional genetic information and may interact differently with other organisms in specific environments. An introduced trait, therefore, cannot be considered in isolation from the biology of the plant into which it is introduced and the environment into which GM crops will be released. Each crop has its own unique characteristics and reproductive biology and these determine how it performs in relation to the environment. Evaluation of the trait with respect to the species and environment is necessary.
The environmental impact of a GM crop compared to a conventionally bred crop can be similar. For example, GM crops that are herbicide and/or pest tolerant exhibit traits similar to those of specific cultivars of wheat (Triticum aestivum L.), maize (Zea mays L.), canola (Brassica napus L.), and soybean [Glycine max (L.) Merr.] that have been developed using conventional technologies. The need to regulate the release of GM crops with these traits, but not those developed using conventional breeding techniques, can appear inconsistent. On the other hand, some GM traits are unique. In the context of a discussion of GM crops and the environment, it should be recognized that regulatory mechanisms provide freedom to experiment and reassurance that the products that are released into the environment have been assessed for their potential risks and benefits. Where this is not clearly understood, results, such as those reported by Ewen and Pusztai (1999), are misinterpreted and ascribed to all GM crops with considerable cost to the credibility of the technology (Royal Society, 1999). Ewen and Pusztai (1999) showed that, under experimental conditions, potato (Solanum tuberosum L.) engineered to contain lectins from snowdrop (Galanthus nivalis L.) might have affected rats (Rattus rattus) during feeding trials. The GM potato was under assessment and had not been released.
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Can Risk and Benefits Associated with These Interactions Be Assessed?
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In conventional breeding programs new crop varieties are often assessed in new/foreign environments before their release. Such assessment is not universal and new varieties can be developed and/or adopted without this assessment in many countries. The assessment process gathers useful information on crop performance and ensures that release of the variety is accompanied by recommendations for on-farm use to maximize benefits. For this reason and as part of the regulatory process, GM trials have been conducted around the world (James, 1998) and attempts have been made to assess the risks and benefits of GM varieties and their impact on the environment.
In many countries scientific assessment of benefits and risks to the environment is required for regulatory compliance. Impact assessment is a tool that can be used in this context and may be applied in conjunction with breeding programs. Evidence required for this assessment includes:
- Effects on human health (see Kaeppler, 2000)
- Effects on nontarget organisms
- Potential for gene escape to wild and/or weedy relatives
- The likelihood that a crop could become a weed in the farming system
As an example, an application for approval to release a herbicide-tolerant lupin (Lupinus angustifolius L.) in Australia necessitated surveys of wild lupin populations, studies of relative flowering times between wild and weedy relatives, and an estimation of outcrossing frequency between transgenic and nontransgenic lupins (Hamblin, 1998). The survival of plants carrying the GM trait was also monitored. In addition, relative performance of the GM variety and conventional variety were studied at several sites; yield, mineral nutrient content of grain, and response to disease were found to be similar (Hamblin, 1998).
Regulatory authorities can require the provision of management plans for use of GM crops (and if necessary associated chemicals) as part of an application for general release (GMAC, 1998; Plant Biotechnology Office, 1999). These plans are designed to minimize risks associated with the new variety and maximize the contribution it can make to sustainable farming. Public perception, particularly in Europe, suggests that introduction of herbicide and pest tolerances, could threaten biodiversity and the intensive European agricultural system (Johnson, 1999). For example, biodiversity might be compromised by changes to agricultural management or the fitness advantage that transgenes transferred to wild relatives could provide. Based on the premise that an open environmental impact assessment process enhances perceptions of integrity, the USDA recently unveiled a Web site with such information at http://www.aphis.usda.gov/biotechnology/.
Observations after release determine the real impact of a new variety on the environment. Although evidence is available of some benefits of GM crops (ERS, 1999), lack of provision for coordinated independent monitoring of key indicators of impact means that benefits and risks remain poorly documented. Commissioned research has been directed toward addressing specific problems (NIAB, 1999). Integration of monitoring and research into programs focused on providing information for risk–benefit analysis is necessary. This is now being undertaken in the UK within an alliance between the government and the Supply Chain Initiative on Modified Agricultural Crops (SCIMAC) (Government of UK, 1999).
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Are There Environmental Benefits from the Technology?
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The majority of GM crops released into production are herbicide tolerant and/or pest resistant (James, 1998). Their introduction in the USA attracted some complaints of poor performance and additional cost (Myerson, 1997). In many cases these reflected a poor choice of varieties used to deploy the trans gene and a reluctance of the biotechnology industry to participate in state- or university-sponsored variety trials, actions that could have helped detect any potential shortcomings in yield before widespread commercialization. Nevertheless, the area under GM crops with these traits has increased in the USA from 3.2 million ha in 1996 to 20 million ha in 1998 (ERS, 1999). Farmers (54–76%) adopted GM crops to "increase yields through improved pest control" (ERS, 1999; Carpenter and Gianessi, 1999).
Increases in yield have been recorded (ERS, 1999) and farmers report a reduction in on-farm costs of agricultural chemicals (Rogers, 1999). Because of annual fluctuations in economic and environmental factors, a decade will be necessary to accurately quantify the impact of insect-resistant crops to the farming sector and the environment. Post release monitoring is therefore important. In Australia, pesticide use on INGARD (Bt) cotton crops has been reduced to about half the number of pesticide sprays used on conventional crops (Pyke, 1999). A reduction in the use of organophosphates in the USA has also been recorded (Rogers, 1999). For cotton farmers in the USA in 1998, the net gain was $92 million, due to both higher yields and reduced insecticide use (Gianessi and Carpenter, 1999). Any reduction in organophosphate usage reduces the impact of these chemicals on nontarget organisms and has positive health consequences for farm workers.
Herbicide usage by American farmers has fallen by 50% (ERS, 1999; Miflin, 1999) as a result of GM crops. Changes in patterns of chemical usage (Rogers, 1999; Gianessi and Carpenter, 2000) can have environmental benefits because individual chemicals have different environmental impacts. An increase in the use of Group G and H (glyphosate and glufosinate ammonium, respectively) herbicides (after incorporating tolerance to these herbicides into crops) and a reduction in Group C herbicides can be beneficial, because the latter are likely to leach into water systems where they are toxic to animals. Group G and H herbicides have high unit activity, tend to bind to soil and break down readily and have relatively low toxicity to animals (Brookes, 1998; Coghlan, 1999; Nottingham, 1998).
Environmental degradation continues to result from human endeavour, including agricultural practices (Cook, 1999). Given that the human population has reached 6 billion, demands on shrinking environmental resources require effective environmental management. Integrated management of agricultural resources including GM crops, pesticides, and herbicides for sustainable production is necessary (James, 1998; Krattiger, 1998). Additional potential benefits from GM crops include their use as tools to limit the impact of industrial activities and for the rehabilitation of toxic waste sites. Production of plastic precursors in plants (Poirier, 1999) and use of genes such as the Mer A gene, which enables GM plants to take up and volatalize mercury (Hg) (Rugh et al., 1998), are pertinent examples.
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Are There Risks to the Environment from the Technology, and Can These Be Managed?
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The opportunity for gene escape and the development of tolerances in weed and pest populations are risks associated with all crops, both conventionally bred and GM crops. Environmental concerns have focused attention on these processes in GM crops with traits such as herbicide and pest tolerance, while conventionally bred crops with similar tolerances have received limited attention in the media.
Gene Escape. Gene escape results from gene flow. This is facilitated by pollen and seed dispersal and provides an opportunity for a trait to move within the same species and to near relatives. Pollen or seed movement is likely to occur at the same frequency in both GM and non-GM crops (Hancock et al., 1996; Raybould and Gray, 1993). Factors affecting gene flow include (Ellstrand, 1992; Hancock et al., 1996; Raybould and Gray, 1993; Moyes and Dale, 1999; Rieger et al., 1999):
- Reproductive barriers
- Modes of pollination
- Methods of seed dispersal (natural and through agricultural activity)
- Genetic stability, fitness, and fertility of hybrids
- Overlap of flowering times
- Proximity and size of populations
- The use of go-between organisms such as fungi, viruses, and aphids
In addition, dispersal as a result of agricultural activities such as spillage during transportation and machinery movements contribute to gene movement and the appearance of novel traits in plants at distances from their release. Survival of an introduced trait depends on the fitness the gene confers on the plant in the new environment. Trans-genes may be introduced into crops selected for their agronomic fitness, a condition that can be detrimental in a nonagronomic environment. The opportunity for trans-genes to move into nonagronomic relatives has the potential to compromise farming systems and biodiversity. This requires careful monitoring where wild weedy relatives of crops are present. In the USA, before a GM crop can be deregulated, the USDA requires evidence that the crop is "unlikely to pose a greater plant pest risk than the unmodified organism from which it was derived." The term pest is further defined to include weediness, either of the plant itself, or of other plants (USDA, 1993).
In many inbreeding crops there is little opportunity for gene flow. Herbicide-tolerant GM crops have provided a tool whereby gene flow can be more accurately measured. There was no detectable cross-pollintation beyond 1.5 m in a GM herbicide-tolerant inbreeding lupin crop (Hamblin, 1998). For outcrossing crops such as canola, rice (Oryza sativa L.), maize, and sugarbeet (Beta vulgaris L.), there is an opportunity for gene flow. For example, canola has a potential outcrossing rate of about 30% (Rieger et al., 1999) and its pollen can be spread over long distances by wind and insects (Scheffler et al., 1995; Moyes and Dale 1999; Rieger et al., 1999). Hybridization between canola and several weed species [e.g., turnip, B. rapa L.; Indian mustard, B. juncea (L.) Czern. & Coss.; and wild radish, Raphanus raphanistrum L.] occurs artificially or under contrived (e.g., using male sterile canola) field conditions, but information is needed on the likelihood of hybridization under normal field conditions and plant densities (Rieger et al., 1999).
Herbicide Tolerance. In many farming systems, outcrossing crops have been grown in conjunction with wild and weedy relatives over long periods of time and the introduction of a GM trait may pose little threat to the farming system. However, even in these systems the introduction of a single trait that confers a strong selective advantage, such as herbicide tolerance, could disturb the balance between the crop and wild and weedy relatives. When such a crop is introduced into an environment in which the weedy relatives threaten the farming system, the risk to sustainable farming is increased. The introduction of triazine-tolerant canola and applications for the release of herbicide-tolerant GM canola have caused concern in southern Australia, where little is known about the potential for gene escape to weedy relatives that are already a threat to the agricultural system. Herbicide-tolerant weeds would severely compromise yields and demand alternative management strategies.
Over use of a particular herbicide and the dominance of a single gene trait may contribute to a loss of effectiveness of herbicide-tolerant GM crops (Powles et al., 1997). Strategic deployment of integrated weed management systems to limit the spread of herbicide tolerance traits within a cropping region is imperative (Bowran et al., 1997). Given the high outcrossing frequencies of canola, problems could also be encountered with the development of multiple resistances in this crop or in weedy relatives. Indian mustard and turnip are not widespread weeds but readily cross with canola. Should they develop herbicide resistance, they could become more widespread (Rieger et al., 1999). Strategic management of the matrix of herbicides and the tolerances to herbicides among the crops (and weeds) in agroecosystems is necessary. To this end, Matthews and Powles (1995) argued for introduction of glyphosate resistance into monocotyledonous crops, and glufosinate resistance into dicotyledonous crops in this farming system. This strategy would reduce the scope for cumulative impacts.
Insect Resistance. Genetically modified crops that carry integral pesticide genes, such as the genes for Bt toxins derived from the bacterium Bacillus thuringiensis, are resistant to a range of insect pests, depending on the specificity of the toxin they carry. The environmental impacts of these plants are recognized risks. Impacts could develop from reduced food supply to predators, such as birds; evolution of resistance to the toxin in target pests; effects on nontarget species and gene escape into the wild, which could improve plant fitness and harm insect populations. Ecosystems could therefore be shifted by escape of such genes. Further, the limited risk of weediness posed by pest-resistant plants currently in farming systems cannot be extrapolated to varieties in which pest resistance genes have been stacked for multiple resistances (Westwood and Traynor, 1999).
Effects of Bt-crops on nontarget species is an issue that has received considerable press coverage since a laboratory experiment showed that Bt corn pollen could compromise the survival of monarch butterfly larvae (Danaus plexippus L.) (Losey et al., 1999). This report has been criticized primarily because laboratory conditions did not reflect field conditions: pollen levels were not representative of those present in the field and the larvae had no choice of feeding materials (Hodgson, 1999). It should also be stressed that impacts on nontarget species are greater and more random where insecticides are sprayed. Indirect effects of Bt toxin, such as effects on predators of target species, also require assessment. In the case of diamondback moths (Plutella xylostella) fed Bt oilseed rape (Brassica napus L.), Schuler et al. (1999b) found that effects on parasitic wasps (Cotesia plutellae) were only indirect, caused by loss of hosts as the moth larvae succumbed to the toxin.
Development of resistance to the Bt toxin in insect populations is considered a risk to conventional and organic farming enterprises. Model systems have been used to study insect resistance to GM crops (Shelton et al., 2000). Establishment of refuge areas adjacent to the crop to reduce selection pressure on susceptible insect populations and the stacking of resistance genes in new varieties are two strategies used to manage this risk. Critics of the refuge concept argue that refuges need to harbor susceptible insects, and farmers aren't used to encouraging insect pests. Furthermore, once a resistant insect is generated, it needs to fly from the Bt crop to the refuge and mate with susceptible insects. As some insects fly only short distances in their lifetime, refuges need to be very close to the Bt crop to be effective. Under these circumstances, the value of refuges in slowing the development of resistance to the toxin could be compromised, especially if resistance is a dominant rather than a recessive trait. Such resistances in insect pests concern organic farmers who rely on biopesticides as part of their pest management strategies. The seed corn industry submitted, and the USEPA accepted, a refuge proposal whereby 20% of the field must be in non-GM corn in regions of the country where cotton (Gossypium hirsutum L.) is not grown and at least 50% for regions where cotton is grown. These refuges must be planted between 0.4 and 0.8 km (0.25 and 0.5 mile) from the Bt corn (NCGA, 2000). The current refuge size for cotton in the USA is 20% if the land is sprayed and 4% if unsprayed, but these sizes may be inadequate (USEPA, 1999). In Australia, the cotton industry has placed an upper limit of 30% on the cotton area to be planted with INGARD cotton (Pyke, 1999).
Virus Resistance. Genetically modified crops of potato, papaya (Carica papaya L.), and squash (Cucurbita spp.), into which viral coat protein genes have been incorporated to increase resistance to viral disease, have been successfully released into the marketplace (Gonsalves, 1998). Nevertheless, two safety issues have been raised over virus-resistant GM crops. First, transgene escape to wild relatives may provide a competitive advantage to these often weedy species. The second concern is for accelerated development of new viruses (Falk and Breuning, 1994). Risk of heteroencapsidation of incoming viruses with coat protein produced by the transgenic plant is a concern, as is opportunity for recombination of the transgene with nucleic acids of incoming viruses. The former could allow nonvectored viruses to become vector transmissible; the latter could create novel viruses (Gonsalves, 1998). Recent studies suggest that complex interactions would be necessary to produce such an outcome (Raybould et al., 1999). Furthermore, similar opportunities for heteroencapsidation and recombination exist in nature wherever two viruses infect the same plant.
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Concluding Remarks
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The GM technology can generate new varieties with traits that might not have been achieved through conventional breeding, and it has the potential to improve the sustainability of farming systems. This is recognized both by farmers and environmentalists, who see benefits in reducing use of chemicals in farming systems and increased yields. Although scientific evidence of the safety of GM crops was presented to regulators before their release, scientists and the public continue to express concern and uncertainty as to the ultimate impact of GM crops on the global environment. This concern can in part be ascribed to a lack of information with respect to how GM crops already released are performing. While logic can be invoked in this debate, there is no substitute for good data. Independent environmental impact assessment and monitoring of specific environmental parameters after release of a GM crop might have seemed unnecessary when GM varieties were first released, but they may have been able to contribute much needed evidence to the current debate. It has been suggested that GM crops introduced into new environments might be assessed in relation to the contribution they can make to sustainable agriculture (Cook, 1999). Cook (1999) offers a list of questions that might be asked before the approval to release a GM crop. These questions are limited by their comparison to existing releases. Reliance on experiences in the environment of first introduction cannot be extrapolated to untrialed environments. Cummulative impacts in the new environment require assessment. Introductions into different agricultural systems could place them at risk. A prior record without ill-effects should not lead to regulatory complacency (Marvier and Kareiva, 1999). Adoption of management systems based on environmental impact assessment in advance of introducing GM crops to farming systems would ensure durability of traits and provide the public with evidence of environmental responsibility. Negative environmental consequences of traditional agricultural practices are not widely communicated, and ignorance of current farming practices and their impacts by the public may prove an obstacle to understanding the need for and acceptance of GM crops (Raybould, 1999). Communication of agronomic and other practices, trends, and limitations in product development at the same time as technological advances can only improve the understanding of the risks and benefits of GM crops to the environment.Government of the United Kingdom 1999; Rural Advancement Foundation International 1999; Schuler Poppy Kerry Denholm 1999
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ACKNOWLEDGMENTS
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The constructive comments provided by Art Diggle and John Hamblin are gratefully acknowledged.
Received for publication January 31, 2000.
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ABSTRACT
INTRODUCTION
