Review Altered pesticide use on transgenic crops and the associated general impact from an environmental perspective

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1 Pest Management Science Pest Manag Sci 63: (2007) Review Altered pesticide use on transgenic crops and the associated general impact from an environmental perspective Gijs A Kleter, 1 Raj Bhula, 2 Kevin Bodnaruk, 3 Elizabeth Carazo, 4 Allan S Felsot, 5 Caroline A Harris, 6 Arata Katayama, 7 Harry A Kuiper, 1 Kenneth D Racke, 8 Baruch Rubin, 9 Yehuda Shevah, 10 Gerald R Stephenson, 11 Keiji Tanaka, 12 John Unsworth, 13 R Donald Wauchope 14 and Sue-Sun Wong 15 1 RIKILT Institute of Food Safety, Wageningen University and Research Centre, Wageningen, Holland 2 Australian Pesticides and Veterinary Medicines Authority, Kingston, ACT, Australia 3 AKC Consultants, Pty, Ltd, West Pymble, NSW, Australia 4 Centro de Investigacion en Contaminaciòn Ambiental (CICA), University of Costa Rica (UCR), San José, Costa Rica 5 Department of Entomology, Washington State University, Richland, WA, USA 6 Exponent International, Ltd, Harrogate, UK 7 EcoTopia Science Institute, Nagoya University, Chikusa, Nagoya, Japan 8 Dow AgroSciences, Indianapolis, IN, USA 9 RH Smith Institute of Plant Science and Genetics, Faculty of Agricultural, Food and Environmental Sciences, Hebrew University of Jerusalem, Rehovot, Israel 10 TAHAL Consulting Eng. Ltd, Tel Aviv, Israel 11 Department of Environmental Biology, University of Guelph, Guelph, ON, Canada 12 Sankyo Co., Ltd, Yasu-gun, Shiga-ken, Japan 13 Private consultant, Chelmsford, Essex, UK 14 University of Georgia Coastal Plain/United States Department of Agriculture Agricultural Research Service, Tifton, GA, USA 15 Taiwan Agricultural Chemicals and Toxic Substances Research Institute, Taichung, Taiwan Abstract: The large-scale commercial cultivation of transgenic crops has undergone a steady increase since their introduction 10 years ago. Most of these crops bear introduced traits that are of agronomic importance, such as herbicide or insect resistance. These traits are likely to impact upon the use of pesticides on these crops, as well as the pesticide market as a whole. Organizations like USDA-ERS and NCFAP monitor the changes in crop pest management associated with the adoption of transgenic crops. As part of an IUPAC project on this topic, recent data are reviewed regarding the alterations in pesticide use that have been observed in practice. Most results indicate a decrease in the amounts of active ingredients applied to transgenic crops compared with conventional crops. In addition, a generic environmental indicator the environmental impact quotient (EIQ) has been applied by these authors and others to estimate the environmental consequences of the altered pesticide use on transgenic crops. The results show that the predicted environmental impact decreases in transgenic crops. With the advent of new types of agronomic trait and crops that have been genetically modified, it is useful to take also their potential environmental impacts into account Society of Chemical Industry Keywords: genetically modified crops; pesticide usage; environmental impact; indicators 1 INTRODUCTION The technology of genetic modification by recombinant DNA has allowed for the transfer of genes, creating transgenic organisms that contain transgenes. A transgene is defined by the authors for the purpose of this study as a gene that has been artificially introduced by recombinant DNA techniques into a site of the genetic material that is different from the origin of the introduced gene, such as from another organism or from a different site in the DNA of the same organism. It is noted that this definition of transgene is broader than that used by some other resources, in that it covers both their definitions of a transgene, i.e. a gene transferred from another organism than the recipient, and a cisgene, i.e. a gene from the same organism. An organism containing a transgene Correspondence to: Gijs A Kleter, RIKILT Institute of Food Safety, Wageningen University and Research Center, PO Box 230, NL-6700AE Wageningen, Holland gijs.kleter@wur.nl (Received 13 December 2006; revised version received 28 February 2007; accepted 4 May 2007) Published online 20 September 2007; Society of Chemical Industry. Pest Manag Sci X/2007/$30.00

2 GA Kleter et al. thus has the property of being transgenic, which is similar to terms such as genetically engineered, genetically manipulated and bioengineered, as well as the term genetically modified used in a narrow sense by some legislations. The first transgenic plants were created in the laboratory in the 1980s, and, later on, in 1996, the first large-scale introduction of commercially cultivated transgenic crops took place. Since then, the adoption of these crops has steadily increased to 102 million ha of land cultivated with these crops in For comparison, this is about twice the total national land surface in Spain. The regions in which the majority of these crops are cultivated include North America, parts of Central and South America, China, India and South Africa. The new traits that have been introduced into the commercial transgenic crops are mainly agronomic, meaning that they primarily target applications for crop protection. The main agronomic traits that are currently associated with transgenic crops are herbicide resistance and insect resistance. Herbicide resistance has been achieved by two mechanisms. Firstly, an enzyme can be introduced that inactivates the herbicide by chemically modifying it. Secondly, if the herbicide s target in the plant is a native enzyme that is inhibited by the action of the herbicide, a mutated form of the target enzyme that is insensitive to inhibition can be introduced. A recent article 2 highlights the current state of herbicide-resistant crops, both transgenic and nontransgenic, and the technicalities and regulatory requirements for the introduction of these crops, including the separate permissions needed in most nations for the use of the herbicide and for the transgenic crop. In addition, it also mentions the double purposes for which herbicide resistance can be used, namely as a marker for development of transgenic crops or as an agronomic trait for weed management. Insect resistance has been achieved by the introduction of insecticidal proteins. In many of the insect-resistant crops that are currently on the market, the insecticidal proteins originate from the soil bacterium Bacillus thuringiensis Berliner. These insecticidal proteins are so-called Cry proteins that occur in crystal-like intracellular inclusions of B. thuringiensis. Preparations of this bacterium have been used for several decades as a biological pesticide, for example in organic agriculture. The advantage over the conventional biological pesticide is that the transgenic protein can be present at low levels in plant tissues over a prolonged period. A recent review highlights the current issues surrounding crops expressing Cry proteins, and also looks forward to possible new transgenic insectresistant crops expressing new Cry proteins, lectins and protease inhibitors, among others. 3 Other traits of agronomic importance in commercial transgenic crops include plant virus resistance and traits that facilitate the breeding of crops, such as combinations of male sterility and fertility restoration. Experimental crops include, for example, plants that have undergone modifications that have rendered them resistant against bacterial and fungal plant pathogens. It is likely that the adoption of transgenic crops with agronomic traits that target crop diseases and pests, such as herbicide and insect resistance, will affect the usage of pesticides, including herbicides and insecticides, on these crops. In 2002, under the supervision of the International Union for Pure and Applied Chemistry (IUPAC), an international team from various fields of crop protection chemistry initiated a project entitled Impact of transgenic crop cultivation on the use of agrochemicals and its environmental consequences. The aim of the project was to make an inventory of the altered pesticide use on transgenic crops compared with that on conventional crops by collecting data from public sources, including scientific literature and reports published by dedicated institutions. At the time of project initiation, a number of studies had been published, including those by team authors 4 and by other authors who focused on the altered use of pesticides on transgenic crops, mainly in terms of quantities of active ingredient and economic effects of transgenic crop adoption. Because pesticides may have different environmental and toxicological properties, changes in quantities used cannot be directly translated into environmental impacts. The project therefore sought to estimate the environmental impact of the observed changes in pesticide usage. During the course of the project ( ), intermediate project results have been published in various conference proceedings. 5 9 This review considers some highlights from these activities and recent findings reported by other authors, particularly on the experience that has accumulated over the years of commercial transgenic crop cultivation and its effect on pesticide use. This complements data considered by several recently published reviews on the impacts of transgenic crop adoption on pesticide use, farm management and other related sectors. 2 ALTERED PESTICIDE USE 2.1 United States of America As stated above, it is likely that pesticide use on transgenic crops with agronomic traits will change. The adoption of transgenic herbicide-resistant soybean in the United States provides an example of this. Data show that the adoption of glyphosateresistant soybean has steadily increased from 1996 onwards, amounting to 89% of total US soybean acreage in 2006 (Fig. 1). Concurrent with this increase in transgenic soybeans, the part of the total acreage of herbicide-treated soybean to which glyphosate is applied one or more times during a growing season has also increased, with a concurrent decrease in the acreage to which other major soybean herbicides are applied (Fig. 2). Note that glyphosate can be used both 1108 Pest Manag Sci 63: (2007)

3 Impact of altered pesticide use on transgenic crops over-the-top on glyphosate-resistant soybean and with directed applications in conventional soybean, so the acreage receiving glyphosate treatments may include both types of soybean. In addition, multiple applications may be given to the same area within the same season, depending, for example, on weed pressure. The same trend as in Fig. 2 is also observed in terms of glyphosate as the fraction of the average amount of herbicide applied to the total acreage of soybeans treated with herbicides (Fig. 3). Various organizations periodically review the usage of pesticide on crops in general and on transgenic crops in particular. In the USA, for example, the Economic Research Service (ERS) of the US Department of Agriculture (USDA) has carried out a number of surveys among farmers since the introduction of transgenic crops into US agriculture. In the surveys carried out by USDA-ERS, selected farms are included and statistical approaches are followed in order to take into account background factors that may influence the farmer s decision to adopt a transgenic crop, such as farmer s income and education level. The ERS-USDA recently published a report on the experiences gained with transgenic crops during the first decade spanning the years of cultivation in the USA. 12 In general, these authors conclude that transgenic crops can have benefits % total soybean acreage herbicide-tolerant soybean adoption, US, '96 '97 '98 '99 '00 '01 '02 '03 '04 '05 '06 year Figure 1. Adoption of transgenic soybeans in the USA, percentage of total acreage. Data from James 33 and NASS. 34 Chlorimuron-ethyl Glyphosate Imazaquin Imazethapyr Pendimethalin Trifluralin l % acreage applied Figure 2. Use of selected herbicides on soybeans in the USA, percentage of total acreage treated with herbicides. Data from NASS; 35 herbicides selected with minimally 10% acreage in 1995; no survey was carried out in kilograms per hectare Glyphosate Non-glyphosate '95 '96 '97 '98 '99 '00 '01 '02 '03 '04 '05 year Figure 3. Herbicide use on soybeans in the USA, average active ingredient per area treated with herbicides, Data from NASS; 35 no survey was carried out in 2003; data have been converted to metric values employing a conversion factor of 1 lb acre 1 = kg ha 1. for the environment thanks to a generally decreased pesticide usage and stimulation of soil conservation practices. Contrary to the generalized downward trend in pesticide usage on transgenic crops, a slight increase in herbicides applied to transgenic herbicide-resistant soybean was observed. However, this increase in herbicides applied to soybean concurs with the shift towards less environmentally persistent herbicides, such as pendimethalin, trifluralin and metolachlor. 13,14 Another organization that regularly publishes surveys on pesticide usage on transgenic crops is the National Center for Food and Agricultural Policy (NCFAP). This Center employs information on pesticide use that it collects from experts in industry, academia and extension services. It has released reports with surveys on actual pesticide use data on transgenic crops in the USA in 2000, 2003 and In addition, NCFAP has predicted the potential impacts of adoption of other, not yet commercialized transgenic crops on pesticide use in Europe and the USA. For example, the actual US data of 2004 included herbicide-resistant canola, cotton, maize and soybean, as well as insect-resistant cotton and maize. 15 The surveys consider the crop protection practices on transgenic crops and possible alternatives for conventional crops in the same year. For herbicide-resistant cotton and soybean, the alternative crop protection measures are considered for each US state, with spray programmes that are attuned to the local circumstances. Virus-resistant papaya and squash were also considered, but were not judged to have impacts on pesticide use. The reductions in quantities of herbicide active ingredients applied to transgenic herbicide-resistant crops are provided in Table 1, showing decreases of 25 33%. In addition, for maize expressing Cry1Ab and Cry1F proteins conveying resistance against corn borers, it was taken into consideration that years of high and low infestation with corn borers can alternate Pest Manag Sci 63: (2007) 1109

4 GA Kleter et al. Table 1. Environmental impact of herbicide use in herbicide-resistant transgenic crops in the United States in 2004 a Item Non-transgenic Transgenic herbicide-resistant Difference Difference, % Herbicide-resistant canola Pesticide use (kg AI ha 1 ) Total impact (EI ha 1 ) Farm worker impact (EI ha 1 ) Consumer impact (EI ha 1 ) Ecology impact (EI ha 1 ) Herbicide-resistant cotton Pesticide use (kg AI ha 1 ) Total impact (EI ha 1 ) Farm worker impact (EI ha 1 ) Consumer impact (EI ha 1 ) Ecology impact (EI ha 1 ) Herbicide-resistant maize Pesticide use (kg AI ha 1 ) Total impact (EI ha 1 ) Farm worker impact (EI ha 1 ) Consumer impact (EI ha 1 ) Ecology impact (EI ha 1 ) Herbicide-resistant soybean Pesticide use (kg AI ha 1 ) Total impact (EI ha 1 ) Farm worker impact (EI ha 1 ) Consumer impact (EI ha 1 ) Ecology impact (EI ha 1 ) a Based on pesticide use data for 2004 from Sankula et al. 15 Units have been converted to metric, e.g. 1 lb AI acre 1 = kg AI ha 1.TheEIQ values have been multiplied by the values of the application rates expressed as kg AI ha 1 in order to calculate the environmental impact per hectare (EI ha 1 ). with each other. Assuming that farmers will only spray insecticide against the target pests in highinfestation years, the authors calculated that adoption of corn-borer-resistant Bt maize would afford savings corresponding to 0.38 lb acre 1 (0.43 kg ha 1 )ina high-infestation year and to 0.17 lb acre 1 (0.19 kg ha 1 ) in a typical year, i.e. the annual average in a 10 year cycle with some years with a high infestation and the remainder with a low infestation. In addition, for cutworm infestation, it was assumed that Bt maize containing the Cry1F protein, which is active against this pest, would have afforded a saving in active insecticide ingredients of 0.20 lb acre 1 (0.24 kg ha 1 ) in selected US states experiencing economic damage. In a similar vein, it was estimated that the adoption of corn-rootworm-resistant maize with the Cry3Bb1 protein would have reduced insecticide treatments by 0.51 lb acre 1 (0.57 kg ha 1 ) of active ingredients. An additional factor besides the built-in insect resistance is seed treatment with insecticides, which obviates the use of soil insecticides that might still be needed against secondary pests in spite of protection against corn rootworm. 15 For insect-resistant cotton, Sankula et al. 15 took into account the fact that a new variety of Bt cotton expressing both the Cry1Ac and Cry2Ab proteins with enhanced protection characteristics against lepidopteran pests had entered the market in It was thus estimated that the Bt cotton expressing Cry1Ac would have led to a decrease by approximately one (0.93) insecticide spray, corresponding to 0.23 lb acre 1 (0.26 kg ha 1 ) of active ingredients. For Bt cotton expressing both Cry1Ac and Cry2Ab, the estimated reduction in pesticides amounted to slightly more than one (1.12) spray corresponding to 0.75 lb acre 1 (0.84 kg ha 1 ) of active ingredients. 15 Brookes and Barfoot 10 used existing data on the farm-level impacts of transgenic crops to calculate the economic and environmental effects of all transgenic crops that had been cultivated over the 9 year period of These crops included herbicideresistant soybeans, maize, cotton and canola, as well as insect-resistant maize and cotton. It thus turned out, among other things, that the adoption of transgenic herbicide and insect-resistant crops has led to a reduction in the total quantities of pesticide ingredients of million kg, corresponding to 6.3% of total active ingredients applied to these crops. This average reduction varies between a reduction of 2.5% for herbicide-resistant maize and 14.7% for insectresistant cotton. 10 Benbrook 16 also considered the changes that the introduction of transgenic crops into US agriculture might have had on pesticide use over the period The findings were based on the data collected by USDA NASS, by other experts and by extrapolation from trends where data were missing. For example, this author found an increase in glyphosate use in glyphosate-resistant soybean, while the conventional soybean acreage showed a trend 1110 Pest Manag Sci 63: (2007)

5 Impact of altered pesticide use on transgenic crops towards lower herbicide use. This latter downward trend was partially explained by the switch to more effective herbicide mixtures that are applied at lower rates, i.e. on average below 0.1 oz AI acre 1 (0.12 kg ha 1 ), and a more restrictive policy on herbicide use. These findings were criticized by Gianessi, 17 for example with regard to differences in the effectiveness of the alternative programmes compared by Benbrook. 16 For herbicide-resistant cotton, Benbrook 16 reports diverging trends towards lower-rate herbicides in conventional cotton and higher rates applied on herbicide-resistant cotton, which in part relates to the occurrence of herbicideresistant weeds, such as marestail showing resistance to glyphosate. Similar conclusions were drawn for herbicide-resistant maize, with the increasing availability of low-rate herbicides and increasing regulatory pressure on high-rate herbicides accounting for a background shift towards lower-rate herbicides in conventional maize. This author also reports that herbicide programmes for glyphosate-resistant maize have been extended with additional conventional herbicide mixtures for increased weed control, which might lead to increased application rates. 16 As regards insect-resistant crops, Benbrook 16 considered the single-gene Bt cotton variety, which still may need bollworm-directed sprays later in the season. In addition, there was a trend towards lower-rate insecticides being applied on conventional cotton. In all seasons considered, Bt cotton received less amounts of pesticides than conventional cotton. For insectresistant maize, it was taken into account that only part of the US maize area is treated with insecticides against corn borers. Although corn-borer-resistant transgenic maize was shown to decrease pesticide used, the potential savings decreased progressively over the years, among other factors because of decreasing application rates of conventional insecticides, which is accounted for by switching to low-rate insecticides for the control of corn borer, such as cyfluthrin Other regions As noted above, various other countries also grow transgenic crops on a large scale, and the data of some recent reports on the effects of pesticide use in these countries are summarized in Table 2. Most of the reports indicate, either in qualitative or in quantitative terms, that pesticide usage decreases following adoption of insect-resistant crops. In one instance, though, the number of herbicide applications is reported to have been increased in herbicideresistant soybean in Argentina. However, the same authors also report that this change concurs with a shift to environmentally more benign herbicides. 18 Interestingly, the studies by Morse et al. 19,20 note that, both in South Africa and India, farmers also sprayed less against non-target pests of Bt cotton, such as plant-sap-sucking insects, probably on the basis of a misunderstanding regarding the target range of Bt crops. However, farmers adopting Bt cotton still experienced a yield revenue, indicating that the bollworm control was more important in this respect. In addition, differences between large and small farmers were also noted in South Africa, with small farmers less prone to use insecticides on conventional maize than large farmers ENVIRONMENTAL IMPACT In order to predict the environmental impact of pesticides used on transgenic crops, it would be useful to combine data on the quantities of pesticides used with data on their environmental and toxicological properties. A method that can be employed for this purpose is the use of environmental indicators that yield outcomes that allow for comparison between different pesticides. An example of such an indicator is the environmental impact quotient (EIQ), which was developed for comparing pesticide programmes in integrated pest management and which has since then been widely used by many international authors for Table 2. Recently reported alterations in pesticide usage on transgenic crops in other countries Change in pesticide use Nation Transgenic crop Trait a seasons Number of Number of applications Amount of AI Costs Reference Argentina Soybean HR 1 +17% 43% 18 China b Rice IR 2 86% 84% 87% 31 India Cotton IR 2 { 54%; 77%} c,d { 72%; 83%} c,d 19 India Cotton IR 1 e e { 50%; 76%} f 32 South Africa Cotton IR 3 e e { 53%; 63%} g 20 South Africa Maize IR 2 e e { 51%; 80%} h 21 a HR = herbicide resistance; IR = insect resistance. b Preproduction farmer trials. c Bollworm insecticides. d Separate data from multiple seasons. e Decrease in pesticide use acknowledged but not quantified in the reference. f Range for four cotton varieties, two official and the other two unofficial varieties. g Range of values from three seasons. h Range of values from three regions. Pest Manag Sci 63: (2007) 1111

6 GA Kleter et al. comparing pesticide programmes. 22 For each active ingredient in a pesticide there is a specific EIQ value based on its toxic properties and environmental behaviour leading to exposure to this pesticide. By multiplying the quantity of a pesticide used, such as the application rate in kg AI ha 1, an abstract value per area unit (ha) is obtained, which constitutes the environmental impact (EI) per acre or per hectare, also called the field use rating. By calculating the EI ha 1 for each pesticide, the outcomes for the various pesticides can be compared with each other. Besides the overall environmental impact, there are also EIQs that cover the impact of pesticides on farm worker health (e.g. dermal contact to plant residues), consumer health (e.g. consumption of residue-containing plant products and drinking water) and ecology (e.g. toxicity to fish, birds, bees and beneficial arthropods). It is noted that some studies have appeared in the literature that describe the effects of pest management in transgenic crops on ecological endpoints, most notably the large-scale farm-scale evaluations (FSEs) that have been performed in the United Kingdom over a 3 year period. The aim was to study the impact of herbicide management in transgenic herbicideresistant canola, maize and sugar beet on weed flora and arthropod diversity within and surrounding the fields. Besides these outcomes, FSE-based studies have also been published on gene flow, statistical field trial design and indicator organisms for future monitoring of agronomic practices. A recent review provides an overview of the chronology and contents of the FSE. 23 The effects studied during the FSE related to the weed management practices and not to the risks of genetic modification per se. In this light, the British Advisory Committee on Releases to the Environment (ACRE) recently recommended evaluating all new farming practices for their environmental impact Calculations performed for the project For the IUPAC project, the EIQ method was applied to the data collected by NCFAP on herbicide use on transgenic and conventional canola, cotton, maize and soybean in the United States in the years 2000, 2003 and 2004 (references 5, 6 and 8 and this publication). Table 1 provides an overview of the outcomes of these calculations on the data of the year As can be observed in this table, both the total quantities ( 30% to 25%) and the environmental impact of herbicides applied to transgenic crops are decreased compared with those applied to conventional crops. This pertains to the general EI ha 1 ( 59% to 39%), as well as to the components for farm worker ( 68% to 40%), consumer ( 59% to 35%) and ecology ( 39% to 55%). Particularly for transgenic herbicide-resistant soybean, the decrease in environmental impact is more pronounced than the reduction in quantities. It should be borne in mind that these data are based on overall data for the USA, and that the conventional and transgenic crop treatments may differ from one locality to another. For example, the NCFAP data for herbicide treatment in soybean considered the appropriate alternative herbicide treatment in each US state. The alternative herbicide treatment with the lowest EI ha 1 value (5.8) was that applied to soybean in South Dakota. The alternative programme consisted of sulfentrazone, cloransulam and quizalofop. Although these active ingredients have EIQs ( ) similar to that of glyphosate (15.3), they are applied at lower rates (0.4 kg AI ha 1 in total) than glyphosate (1.06 kg AI ha 1 ), for which the value of the environmental impact (EI ha 1 ) amounted to These outcomes are in line with those calculated using the same method for usage data of previous years (2000, 2003) in the USA, showing that both the amount and the impact of active herbicide ingredients applied to transgenic crops decreased compared with alternative programmes for conventional crops. 3.2 Reports in the literature Retrospective analysis As mentioned above, Brookes and Barfoot 10 performed a retrospective analysis of the global pesticide usage on transgenic crops during the period These authors also applied a calculation of the footprint of the pesticides used by applying the EIQ to the quantities of pesticides used, as considered for each specific crop and nation of cultivation. The results thus showed that the 6.3% decrease in overall quantities of active ingredients was accompanied with a 13.8% decrease in EI per area unit, varying between 3.4% for transgenic herbicide-resistant maize and 21.7% for transgenic herbicide-resistant cotton. For each transgenic crop, the effect on the EI per area was greater than on quantities of active ingredient, most notably for herbicide-resistant soybeans, for which a 3.8% decrease in active ingredients concurred with a 19.4% decrease in environmental impact. 10 Brimner et al. 9 considered the changes in herbicide use on canola (oilseed rape) in Canada during the period , in the course of which, in 1996, the introduction of herbicide-resistant varieties took place. Herbicide-resistant canola varieties are currently cultivated in Canada on a large scale, including transgenic varieties that are glyphosate- and glufosinate-resistant and non-transgenic imidazolinone-resistant varieties. For the estimation of the quantities of herbicides applied, the reported acreage treated with the specific herbicides was multiplied with the minimum rates recommended for the application of these herbicides. The results show that the kinds of herbicide used have changed substantially over the period considered. In addition, the environmental impact of herbicide use in Canadian canola was estimated according to the EIQ methodology. The results thus showed that the lower impact of herbicides used on herbicide-resistant canola caused a decrease of 36.8% in the overall impact of herbicides used on all canola in the period Pest Manag Sci 63: (2007)

7 Impact of altered pesticide use on transgenic crops Knox et al. 25 also employed the EIQ methodology in order to estimate the environmental impact of the introduction of insect-resistant transgenic cotton ( Bt cotton ) expressing insecticidal proteins originating from B. thuringiensis in Australia. Two types of Bt cotton were considered, the first containing the Cry1Ac protein and the other one containing a combination of Cry1Ac and Cry2Ab, of which the latter had been grown since Pesticide usage data from surveys, covering seven seasons in the period , were used, enabling the analysis of chronological developments. Interestingly, the calculations also included the estimated effect of the transgenic insecticidal proteins present in plant residues, which were shown to have comparatively little effect on the overall outcomes. It was thus observed that Bt cotton exerted less environmental impact than conventional cotton, with the impact of the Cry1Ac cotton being on average 53% and that of the Cry1Ac and Cry2Ab being 23% of that of conventional cotton. In addition, there was some variability in the environmental impact of Bt cotton between years owing to differences in pest pressure Prospective analysis Peterson and Shama 26 compared the potential environmental and health effects of transgenic herbicide (glyphosate)-resistant, non-transgenic herbicide (imidazolinone)-resistant and conventional wheat based on toxicity data of the herbicides. The imidazolinone herbicide was imazamox, and the conventional group included 15 herbicides that are commonly used in spring wheat in Northern America. The glyphosateresistant wheat has not yet been introduced onto the market given that the company developing this transgenic wheat decided to focus on other crops owing to the comparatively better market prospects for these crops. 27 Therefore, the study can be considered prospective. Consumer exposure to herbicides was estimated by combining the maximum residue levels with the average consumption of wheat-containing foods. This intake was used to compare it with the acceptable daily intake and to calculate the lifetime cancer risk using the tumour potency factor for the given herbicide, if applicable (not for glyphosate). In addition, applicator risk associated with estimated dermal exposure, and assessed with the aid of previously described computer simulation models, and ecological risks for non-target terrestrial plants, aquatic organisms and groundwater were considered. The results thus showed that the relative risks of exposure to glyphosate and imazamox with respect to the toxicity endpoints were favourable for each effect in comparison with many of the other, conventional herbicides DISCUSSION The first decade of transgenic crop cultivation has witnessed a steady increase in the area planted with commercial transgenic crops and the number of countries in which these crops are grown. A limited number of crops make up the majority of these transgenic crops, and the traits that have been introduced into these crops are mainly of agronomic interest, such as herbicide and insect resistance. Most of the data collected on pesticide use in these crops indicate that there is a decrease in the amounts of pesticides applied to these crops. In addition, it is noteworthy that many of the non-anecdotal data that have been collected on realworld pesticide use on transgenic crops and that were considered useful for the purpose of the study pertain to the situation in North America. This may be accounted for by the fact that more than half of the transgenic crops are currently grown in this region. In addition, a number of authors, including those affiliated with NCFAP and USDA, and Dr Benbrook, also collect relevant detailed information on the regional pesticide use on a regular basis, the results of which are published in accessible media. The lesser availability of data on pesticide use on transgenic crops outside North America may relate to lower accessibility of data and less experience with growing transgenic crops, among other factors. However, quantities alone may not be sufficient to predict the environmental consequences, given that the new and old pesticides may each have their own toxicity profile and environmental behaviour. A universal indicator, the EIQ, was therefore employed to relate the quantities of a particular pesticide to its environmental effects, in order to be able to compare the environmental impacts of pesticide programmes applied to transgenic crops and their conventional counterparts. The results of these calculations show that the environmental impact also decreases upon adoption of transgenic crops, which can be more pronounced than the reduction in active ingredients applied to the crops. The EIQ is a universal indicator that encompasses consumer, farm worker and ecology aspects. For some purposes, other types of indicator may also be useful, such as concentrations in surface water or monetary effects of environmental contamination with pesticide residues (e.g. as reviewed by Levitan et al. 28 ). These were, however, beyond the scope of the present review. Transgenic crops may also have an impact on the environment through secondary effects. For example, the introduction of herbicide-resistant soybeans in the USA is correlated with an increase in reducedor no-tillage activities in the soybean fields. This in turn may be beneficial for erosion-sensitive soils, for example. 29 Another example is the incorporation of transgenic insect-resistant crops into integrated pest management schemes, as has been done with Bt cottonintheusstateofarizona. 30 Because of the built-in resistance to certain lepidopteran pests, broadspectrum pesticide sprays in the early season may be obviated. Beneficial insects and natural enemies of plant pests thus would have the chance to establish Pest Manag Sci 63: (2007) 1113

8 GA Kleter et al. themselves in the crop, which may further lead to pesticide reductions, creating a win-win situation. The overall results of this study therefore indicate that positive benefits can be achieved through the use of the crop traits of insect resistance and herbicide resistance. Whereas the focus has been on transgenic crops, it can be envisioned that, in some cases, similar traits could also be obtained through other than transgenic breeding technologies, as in the case of imidazolinone-resistant crops. Furthermore, in the near future, crops with other agronomic traits may be introduced that are likely to have a large impact on agrochemical use as well, such as the development of blight-resistant potatoes, which could afford savings on fungicides applied against Phytophthora. Also, the range of crops may be extended. Both from a scientific and from a policy-based point of view, it would be useful to keep track of the ongoing developments and to estimate the associated impact on the environment. ACKNOWLEDGEMENTS Financial support from the International Union for Pure and Applied Chemistry and the Dutch Ministry of Agriculture, Nature and Food Quality is gratefully acknowledged. REFERENCES 1JamesC, Executive Summary of Global Status of Commercialized Biotech/GM Crops in [Online]. ISAAA Briefs No. 35, International Service for the Acquisition of Agri-Biotech Applications, Ithaca, NY (2005). Available: executivesummary/default.html [17 February 2007]. 2 Devine MD, Why are there not more herbicide-tolerant crops? Pest Manag Sci 61: (2005). 3 Christou P, Capell T, Kohli A, Gatehouse JA and Gatehouse AMR, Recent developments and future prospects in insect pest control in transgenic crops. 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