- IntroductionThis subsection provides a short review of the potential environmental impacts of GM crops.Some commonly expressed environmental concerns about GM crops are: 1) gene flow between the transgenic plants and their sexually compatible relatives, 2) changes in levels of weediness or invasiveness of the GM crops or their wild relatives; 3) horizontal transfer of engineered traits to other species, 4) non-target effects and 5) development of pest resistance or new secondary pests.
- Genetically Modified Crops and Gene FlowGene flow refers to the transfer and incorporation of genes from one population into another through pollen or seed movement (Andow and Zahlen, 2005). Pollen movement is not by itself an environmental concern, unless the GM crop can successfully hybridize with a relative.Hybridization occurs frequently between crops plants and their sexually compatible relatives (both crops and wild species). Ellstrand et al. (1999) gave many examples of natural inter-hybridization among the most important crops cultivated in the world. These include rice (Oryza sativa and Oryzaglaberrima ), maize (Zea mays), sorghum (Sorghum bicolor), cotton (Gossypium hirsutum and Gossypium barbadense), millets (Pennisetum glaucum), sugarcane (Saccharum officinarum) and groundnut (Arachis hypogea). These are of particular importance in Africa as staple and cash crops.While hybridization between crops and their relatives is a common phenomenon, a number of factors must take place for gene flow to occur. Plant species must 1) be sexually compatible, 2) close enough for the pollen to be moved between plants by wind or vectors such as insects or birds, and 3) be in flower at the same time (Ellstrand et al. 1999). Similar to their non GM counterparts, GM crops will probably hybridize with their sexually compatible species if they are grown in close proximity. For example, Lu (2008) showed that hybridization between transgenic and weedy rice (Oryza f. spontanea) is unavoidable where they co-exist and that the insect-resistant Bt transgenes can be incorporated and persist in the weedy rice populations.
Hybridization between GM crops and their compatible relatives may or may not have environmental consequences. The impact of transgenes on natural populations is determined by the combination of the trait expressed by the gene itself and the invasiveness of the recipient species (Hancock, 2003, Nickson, 2008).
- Changes in Levels of Weediness or InvasivenessConcerns have been raised that 1) transgenic crops themselves could become weeds and invade agricultural or natural ecosystems, and 2) the engineered traits could be introduced into wild relatives via hybridization and increase the competitive ability and the weediness of those wild plants or their hybrid derivatives. Thus, the risk of generating increased weediness has been a major environmental concern associated with transgene flow.What is considered a weed differs according to eco-geographical regions and whether agronomic fields or natural plant communities are considered. Ellstrand et al. (1999) defined weeds as “wild plants that interfere with human objectives”; and wild plants as “plants that grow and reproduce without being deliberately planted.” USDA APHIS (2008) considers a noxious weeds as “any plant or plant product that can directly or indirectly injure or cause damage to crops, (–), or other interests of agriculture, irrigation, navigation, the natural resources, the public health, or the environment.”Different weed species share some common ecological and biological attributes such as preference for disturbed habitats (cultivated fields, roadsides, fields margins, soil dumps), phenotypic plasticity allowing for adaptation to changing environments, low seed dormancy, indeterminate growth, continuous flowering and high seed production (Conner et al., 2003). However, the most critical predictors of the weediness of a given plant are (OGTR, 2003): “1) its taxonomic affinity to other known weedy species and 2) its history of weediness elsewhere in the world.”
Many of the GM crops developed so far such as cotton, maize and soybean have been selected for thousands years by humans on agronomic sites and have lost many of their weedy characters. In fact, only a small percentage of agronomic crops are important weeds outside of agro-environments (Hancock and Hokanson, 2004; Hancock, 2003). They rely on human disturbances to become established and rarely persist outside of specific habitats. This means that the addition of the transgenes now commonly deployed is unlikely to make them noxious weeds (Conner et al., 2003). Thus, GM crops are not more likely to become weeds than their non-GM counterparts (Conner et al., 2003).
The bottom line in assessing the environmental risk of GM crops is the nature of the transgene itself, that is, how significant impact it will have on the reproductive potential of native populations should it escape (see section above on risk assessment). In fact, it is much easier to predict the environmental risk of a GM crop, than that of an exotic plant introduction, as the level of risk in GM crops can be measured by evaluating the impact of a single engineered trait than a whole syndrome of potentially invasive traits found in an exotic species. The GM crop is already in the environment that it is traditionally grown, and we know the evasiveness of the traditional crop. What we need to worry about is whether the addition of a single GM trait will increase its existing level of invasiveness to problem levels.
Concerns have been expressed about crops that contain herbicide tolerance genes turning into uncontrollable weeds, particularly if several crops of the same species and tolerant to different herbicides are grown in close proximity. Multiple hybridizations can therefore occur and may result in multi-herbicide resistant hybrids which are difficult to eradicate (McHughen, 2000). Studies in Canada have already revealed the presence of oilseed rape plants that had became tolerant to three different herbicides following hybridization with two GM herbicide tolerant varieties and a conventional one (Dale et al., 2002). It is important to realize that while the emergence of herbicide resistance in weed species could add to farm management burdens, it will not impact on the natural environment where herbicides are not applied.
Hybridization between wild species and transgenic insect or disease resistant varieties may also result in populations with increased fitness, but only if the target pests were typically controlling the natural population size of the wild relatives. For instance, because of reduced effects of LepidopteransHelianthus annus) have been shown to produce 14 – 55% more seeds (Snow et al., 2003). However, it is important to remember that an increase in fitness of individuals will not necessary lead to change in the population size of a given wild plant species. Density dependent selection can still keep population sizes the same, by increasing the mortality rates of additional individuals (Raybould and Cooper, 2005).
- Horizontal Transfer of Engineered Traits to Other SpeciesHorizontal gene transfer is defined as a stable transfer of genetic material from one organism to another without reproduction or human intervention (Kesse, 2008). This phenomenon can occur between bacteria and is considered a significant source of genome variation (Conner et al., 2003). Concerns have been raised that engineered traits could be transferred to non-target organisms via horizontal transfer and thereby threaten environmental and animal safety (Droge et al., 1998, 1999).This topic has received considerable attention from numerous expert panels held under the auspices of various national and regional regulatory systems as well as international bodies such as OECD, WHO or FAO. Based on scientific evidence, they report that horizontal gene transfer from GM plants to other organisms is, at most, an extremely rare phenomena and to date no environmental harm has been reported from it (Nielsen et al., 1997; 1998, 200b; 2007, Schluter et al., 1995; Anderson, 2005, Gebhard and Smalla, 1998; Mercer et al., 1999, Lambert and al., 1999; Bird and Koltai, 2000, Simpson et al., 2007, Kesse, 2008). The European Food Safety Authority (EFSA) has confirmed that the nptII gene commonly used as a selectable marker in GM crops does not pose a risk to humans or the environment: http://www.efsa.europa.eu/EFSA/efsa_locale-1178620753812_1178620789287.htm, http://www.efsa.europa.eu/EFSA/efsa_locale-1178620753812_1178620775641.htm
- GM Crops and BiodiversityBiodiversity refers to “the variability among living organisms from all sources, including, among others, terrestrial, marine and other aquatic ecosystems and the ecological complexes of which they are part; this includes diversity within species, between species and of ecosystems” (Convention of Biological Diversity, 1992). Biodiversity is represented by both numbers of species and genetic variability within the species.Concerns have been raised that the wide spread of GM crops could adversely affect the levels of natural diversity through: 1) replacement of traditional varieties (land races), 2) hybridizations between GM crops and land races or wild relatives, particularly in “centers of diversity” and 3) interactions with non-target organisms. Land races and centers of diversity are of particular importance both to farmers and plant breeders as sources of food and storehouses for genetic diversity to improve crop varieties.Hybridization between GM crops and wild relatives could reduce levels of genetic variability through two routes: 1) a native population could go extinct due to high levels of pollen flow from a much larger commercial field, or 2) selectively advantageous crop genes could replace native ones through hybridization.
Extinction could occur if such high numbers of fertile hybrids are formed that they ultimately replace the pure native types. While there are no reports of crop/wild hybridizations leading to the extinction of a whole species, there have been instances where hybridization has resulted in the extinction of local populations (Ellstrand et al., 1999).
Genes in native populations could be replaced by transgenes through gene flow, if hybrids are formed and the transgene is gradually incorporated into the recipient population through backcrossing. Whether the transgene persists in the native population and has an impact on the range or fitness of a native population is associated with the phenotypic effect of the gene itself and the invasiveness of the recipient species (see next section). The transgenes most likely to be incorporated are those that confer a selective advantage.
The risk of altering native levels of genetic diversity via pollen flow is not unique to GM crops and is associated with the large scale cultivation of any new crop species. The presence of the transgene is the only difference associated with the GM crops (Hancock, 2009). While traditional varieties have been replaced in some areas by commercial varieties, traditional varieties have been maintained in many others, suggesting that farmers can keep land races pure if they so desire (Gepts, 2004; Perales et al., 2003; Bellon and Berthaud, 2004).
GM Crops and Centers of Diversity
Concerns have been raised that the planting of transgenic crops in “centers of species diversity” could result in losses of genetic variability (Rissler and Mellon, 1996; Gepts and Papa, 2003; Gepts, 2005). The most often expressed concern relates to sexual hybridization between the transgenic crop and its relative, and the possibility that levels of genetic diversity will be reduced from that interaction, and in the worst case senerio, that natural populations or land races might go extinct.
The potential ramifications of crop/species gene flow are of concern because landraces are important food sources to many indigenous peoples, and the centers of diversity are considered to be important storehouses of the raw genetic material necessary for breeding new characteristics into crops. Of course, the risk of losing a native population to gene flow from a transgenic crop is fundamentally no different than that possessed by conventionally bred crops. The only difference is the presence of the transgene.
In reality, most crop progenitors are dispersed over a wide geographical range and their numbers are large, so the likelihood of their species extinction is minimal. In many cases, it is also difficult to find single centers of crop diversity. Some crops have multiple centers diversity (wheat, sorghum, pearl millet, barley, pea, lentil, chickpea, flax, maize and lima bean), and some have no discernible centers of diversity at all (radish, sorghum, pearl millet, cole crops and bottle gourd) (Harlan 1995, 1976 and 1992).
Paradoxically, hybridization between crops and wild species, could actually result in higher levels of genetic diversity in the wild relative as the genes of the wild species and the crop are blended together. As the new taxon evolves, many alleles will be lost, but the hybrid population is likely to carry high levels of diversity for many generations.
- Impact on Non-Target OrganismsNon-target organisms are any organisms that may be adversely affected by the GM crops that were not the intended targets. For example, a crop may be engineered for resistance to a specific insect pest (the target) and any other insects would be non-target organisms. These include various taxa that “fulfill important ecological functions such as biological control, pollination and decomposition” (Romeis et al., 2008). Craig et al, (2008) classifies the non-target organisms into “1) pollinators and natural enemies of pest and the wider category of beneficial species, 2) soil organisms, 3) non-target herbivores, 4) endangered and other species of conservation concern, 5) species which contribute to local biodiversity.”Non-target organisms are a concern in risk assessment, only if the crop has been engineered with a toxin that makes it insect resistant and there are other organisms that might be sensitive to it. Non-target organisms are not of concern if the crop has been engineered for traits that will not affect organisms other than the crop, such as herbicide resistance, virus tolerance or drought tolerance.Potential direct and indirect effects of GM plants on non target organisms have been described (Conner et al., 2003). Direct effects are due to toxicity through ingestion by the non-target organisms of a toxin produced by the GM plant, e.g. other insects feeding on Bt plants. Indirect effects occur via multi-trophic food chains, involving, for example, organisms not directly consuming the GM plant but feeding on other insects associated with the transgenic plants (Conner et al., 2003, Craig et al., 2008).
Of the GM crops currently on the market, Bt crops are those with potential for non-target impacts; so the effects of Bt proteins have been extensively evaluated. Results from a number of those studies have been summarized by OECD (2007) in a consensus document on “Safety Information on Transgenic Plants expressing Baccillus thuringiensis – derived insect control protein.” The broad concensus is that few non-target organisms are negatively impacted by exposure to Bt proteins. Poultry, for instance, was not adversely affected when fed with maize expressing Cry34Ab1 and Cry35Ab1. Likewise, the fresh water daphnia (Daphnia magna) exposed to the Cry34Ab1/ Cry35Ab1 was not negatively affected as well as soil micro-organisms and macro-organisms (protozoa, fungi, bacteria, nematodes, earthworms) in Cry1Ab maize field. No effects were seen on honeybee (Apis mellifera) larvae and adults fed pollen containing proteins of Cry1Ab, Cry1Ac, Cry9C Cry3A, Cry2Ab2, Cry3Bb1, Cry34Ab, Cry35Ab1. In another study, aphids that play an important role in agricultural systems, as prey or host to a number of predators and parasitoids were shown to be unaffected by Bt cotton in India (Lawo et al. 2009). Larvae of the Monarch butterfly (Danaus plexippus) can be adversely impacted when they ingest high amounts of Bt pollen ( they belong to the same Lepidoptera order targeted by some of the Bt crops); however, native population sizes of this insect are little affected by the widespread growing of Bt corn, as few insects receive toxic levels in the field. Mammals are not affected by the consumption of Bt, as they lack the specific receptors to which Bt endotoxins bind.
It should be noted that the higher yield gained from GM crops could actually reduce the conversion of rich forest into farmlands, and thereby protect the biodiversity hosted in those ecosystems (Clive, 2009). Also, the specificity of certain GM proteins such as Bt proteins has reduced the use of hasher pesticides that are toxic to many more species. In fact, earthworms, bees and beetles have been found more abundant in Bt cotton fields than in conventional sprayed fields (Marvier et al., 2007).
- Other Agro-Ecological ImpactsResistance to Bt ToxinsThe widespread cultivation of pest-resistant GM crops might lead to resistance developing in the targeted pests. This is, of course, a risk to product performance, not the environment.Resistance to Bt has been reported in three Lepidopteran species in three countries: 1) South Africa in 2006 for resistance of stem borer (Busseolafusca) to Cry1Ab corn, 2) Puerto Rico in 2006 for resistance of fall armyworm (Spodoptera frugiperda) to Cry1F corn, and 3) USA in 2003 for resistance of bollworm (Helicoverpa zea) to Cry1Ac cotton (Tabashnik et al., 2008, Biosafety Assessment Tool, Centre for Biosafety, http://bat.genok.org/bat/).
Management strategies have been developed to delay the evolution of resistance in pest populations. Typically, these involve high doses of the pesticidal protein expressed by the transgenic plant, in conjunction with a refuge that is planted alongside the transgenic crop field. A refuge is an area planted with a similar non-transgenic crop which does not express the specific toxin. Its purpose is to maintain a population of the target insects that possess alleles for susceptibility to the transgenic protein. When the susceptible insects mate with resistant individuals, the level of resistance is reduced in the progeny. The high dose/refuge strategy is based on certain assumptions about the target pest genetics, including 1) resistance is a susceptible trait, 2) resistance is rare, 3) mating is random.
Overall, the evolution of resistance remains an important concern that must be continually addressed. The emergence of resistance will impact primarily on the control of pests in farmers’ fields and may cause a return to control strategies currently employed in non GM crops fields which are less friendly to the environment.
Resistant Weeds to Glyphosate Herbicide
In recent years, glyphosate resistant weeds have also been reported in some countries (Duke and Sanderman, 2006; Service, 2007). In the USA for instance, corn and soybean growers recently reported on weeds that had developed resistance to Roundup (Kruger et al., 2009). These weeds include giant ragweed (Ambrosia trifida) which is one of the weeds that drove the adoption of Roundup (Kruger et al., 2009). Other reports of resistance to glyphosate include Sorghum halepense (Johnsongrass) in Argentina and USA; Lolium spp (ryegrass) in USA and Australia, Amaranthuspalmeri, Amaranthus rudis and Amaranthus tuberculatus (waterhemp) in USA; Euphorbia heterophylla in Brazil; Conyza canadensis (horseweed) in both Brazil and China (Biosafety Assessment Tool, – Centre for Biosafety, http://bat.genok.org/bat/).
Losing the use of glyphosate would be a critical issue if it brought back the use of herbicides that are less friendly to the environment. However, management strategies have been developed to delay the development of resistance, including rotating the use of different herbicides (Kruger et al., 2009), and using “stacked” GM plants that have tolerance to more than one herbicide. However, gene flow from stacked plants to native relatives could lead to the development of multi-resistant weeds (Biosafety Assessment Tool, – Centre for Biosafety, http://bat.genok.org/bat/). This raises agricultural concerns; however it is not an environmental issue as herbicides are not spayed in natural environments.
Conner, J. A., Glare, R. T, and Nap, J-P, 2003. The release of genetically modified crops into the environment, part: Overview of ecological risk assessment. The Plant Journal 33, 19-46.
Convention of Biological Diversity, 1992 : http://www.cbd.int/convention/refrhandbook.shtml
Craig, W., Tepfer, M., Degrassi, G., Ripandelli, D., 2008. An overview of general features of risk assessments of genetically modified crops. Euphytica
Dale, P. J., Clarke, B., Fontes, M. G. E., 2002. Potential for the environmental impact of transgenic crops. Nature biotechnology, 20, 567-574.
European Food Safety Agency (EFSA) guidance documents : http://www.efsa.europa.eu/en/gmo/gmoguidance.htm
Ellstrand, N. C., Prentice, H. C. and Hancock, J. F., 1999. Gene flow and introgression from domesticated plants into their wild relatives. Annu. Rev. Ecol. Syst., 30, 539-563.
Ellstrand, N. C., 2001. When transgenes wander, should we worry? Pl. Physiol., 125, 1543-1545.
Ellstrand, N. C., 2003. Dangerous liaisons? When cultivated plants mate with their wild relatives. The John Hopkins University Press, Baltimore, MD.
FAO/WHO, 2000. Safety aspects of genetically modified foods of plant origin. Report of a Joint FAO/WHO Expert Consultation on Foods Derived from Biotechnology. World Health Organization, Headquarters Geneva, Switzerland. 29 May – 2 June 2000
Gepts, P., 2005. Introduction of transgenic crops in Centers of origin and domestication. In: D.L. Kleinman, A.J. Kinchy and J. Handelsman (eds.) Controversies in science and technology from maize to menophase. University of Wisconsin Press, Madison.
Gepts, P. and Papa, R., 2003. Possible effects of (trans)gene flow from crops on the genetic diversity from landraces and wild relatives. Envir.Biosafety Res. 2: 89-103.
Hancock, J. F. and Halsey, M., 2009. Control and monitoring of gene flow from genetically engineered crops to relatives. Michigan State University. In press.
Hancock, J. F, 2009. Factors influencing the genetic diversity of crop species and the impact of transgene escape. Michigan State University. In press.
Hancock, J. F., 2003. A framework for assessing the risk of transgenic crops. BioScience 53:512-519.
Hancock, J. F. and Hokanson, K., 2004. Invasiveness of transgenic vs. exotic plant species: How useful is the analogy. In: S. H. Strauss and H. D. Bradshaw (eds.). The Bioengineered Forest: Challenges for Science and Technology. RFF Press, Corvallis, Oregon.
Harlan, J.R., 1992. Crops and man. Second edition. American Society of Agronomy, Madison, Wisconsin.
James, C, 2009. Global Status of Commercialized Biotech/GM Crops: 2008 The First Thirteen Years, 1996 to 2008. ISAAA Brief. 39, Executive Summary. ISAAA: Ithaca, NY.
Kesse, P., 2008. Risks from GMOs due to Horizontal Gene Transfer. Environ. Biosafety Res. 7. 123-149.
Kruger, R. G., Johnson, G. W., Weller, C. S., Owen, D. K. M., Shaw R. D., Wilcut, W. J., Jordan, L. D., Wilson, G. R., Bernards, L. M. and Young, B. G., 2009. U.S. Grower Views on problematic Weeds and Changes in Weed Pressure in Glyphosate-Resistant Corn, Cotton, and Soybean Cropping Systems : http://news.uns.purdue.edu/x/2009a/090414JohnsonSurvey.html
Lawo, N.C., Wäckers, F.L.and Romeis, J., 2009. Indian Bt cotton varieties do not affect the performance of cotton Aphids. PLoS ONE 4(3): e4804. doi:10.1371/ journal.pone.0004804
Lu, B. R., 2008. The fitness of hybrids and progenies between weedy rice and insect-resistant Bt (cry1AC) rice. International Symposium of the Biosafety of Genetically Modified Organisms, 10th, November 2008.
Marvier, M., McCreedy, C., Regetz, J. and Kareiva, P., 2007. A meta-analysis of effects of Bt cotton and maize on nontarget invertebrates. Science 316: 1475-1477.
Nielsen, K. M., Gebhard, F., Smalla, K., Bones, A.M., Van Elsas, J.D., 1997. Evaluation of possible horizontal gene transfer from transgenic plants to the soil bacterium Acinetobacter calcoaceticus BD413 Bio/Technology 13, 1094 – 1098 (1995)
Nielsen, K.M., Bones, A.M., Smalla, K., Van Elsas, J.D., 1998. Horizontal gene transfer from transgenic plants to terrestrial bacteria – a rare event? FEMS Microbiol. Rev. 22: 79-103.
Organisation for Economic Co-operation and Development (OECD), 2006. Safety Assessment of Transgenic Organisms. OECD Consensus Documents Volume 1. ISBN 92-64-02258-9
Organisation for Economic Co-operation and Development (OECD), 2007. Consensus Document on Safety Information on Transgenic Plants Expressing Bacillus Thuringiensis-Derived Insect Control Protein. Env/JM/MONO(2007)14.
Office of the Gene Technology Regulator (OGTR), 2003. The Biology and Ecology of Papaya (paw paw), Carica papaya L., in Australia : http://www.ogtr.gov.au/internet/ogtr/publishing.nsf/Content/papaya-3/
Raybould, A., Cooper, I., 2005. Tiered tests to assess the environmental risk of fitness changes in hybrids between transgenic crops and wild relatives: the example of virus resistant Brassica napus. Environ. Biosafety Res. 4, 127-140.
Romeis, J., Bartsch, D., Bigler, F., Candolfi, M.P., Gielkens, M.M.C., Hartley, S.E., Hellmich, R.L., Huesing, J.E., Jepson, P.C., Layton, R., Quemada, H., Raybould, A., Rose, R.I., Schiemann, J., Sears, M.K., Shelton, A.M., Sweet, J., Vaituzis, Z. & Wolt, J.D., 2008. Assessment of risk of insect-resistant transgenic crops to nontarget arthropods. Nat Biotechnol. 26, 203-208.
Schlüter, K., Fütterer, J., Potrykus, I., 1995. “Horizontal” Gene Transfer from a Transgenic Potato Line to a Bacterial Pathogen (Erwiniachrysanthemi) Occurs—if at All—at an Extremely Low Frequency. Bio/Technology 13, 1094 – 1098
USA APHIS, 2008. Importation, Interstate Movement, and Release into the Environment of Certain Genetically Engineered Organisms. Docket No. APHIS-2008-0023 : http://www.regulations.gov/search/Regs/home.html#docketDetail?R=APHIS-2008-0023
Dr Moussa Savadogo,
ABNE Senior Program Officer
Environnemental Biosafety Specialist