- Email: [email protected]
GM crops: environmental risks and non-target effects
trends in plant science Meeting Report Clearly, transcription factors induced under a particular stress condition, such as Atf1 and Pap1 in fission yeast, regulate the expression of many proteins (‘operons’), including general antioxidant enzymes, metabolic enzymes, regulatory elements and structural proteins. The induction of drug resistance in E. coli after the induction of the SoxS regulon under oxidative stress (Daniële Touati), and the regulation of multiple stress genes in Arabidopsis under osmotic stress (Nicole Verbruggen, University of Gent, Belgium), are further demonstrations of the complex interaction between stress–resistance phenomena. This high level of complexity was particularly clear from proteome, transcriptome and multi-gene array analyses. A single osmotic shock in yeast cells resulted in the altered expression of .280 genes (Stefan Hohmann) and oxidative stress induced by methylviologen treatment in leaf material induced the expression or suppression of .120 genes (Dirk Inzé, University of Gent, Belgium). Stress signal sensing
In contrast with the rapidly accumulating knowledge on signal transduction, relatively little is known about how cells sense oxidative or osmotic stress signals. In yeast, the Sln1 protein is involved in the perception of osmotic stress (Francesc Posas). It is com-
posed of an extracellular sensory domain and a cytoplasmic histidine kinase domain, and potentially functions as a classical ‘two component’ sensor in the induction of the HOG1 pathway. AtHK1 in Arabidopsis shows homology to Sln1, and can function as an osmosensor in yeast. At present, it is hypothesized that osmotic stress-induced cell size changes might exert increased lateral pressure on the membrane-spanning osmosensors, and thereby bring about conformational changes and activation of the kinases. Thought provoking questions
Two workshop sessions were organized to promote the exchange of ideas and viewpoints between researchers from the different fields. Although it is often difficult to animate group sessions, the discussion leaders Dennis Thiele (University of Michigan, USA) and Stefan Hohmann provided several thought provoking questions. For example, the question was raised, whether induction of a certain set of stress genes might also lead to cross protection against other stresses. To date, only a few results point in this direction, therefore this question requires further investigations before it can be answered. The discussion also emphasized the dual function of reactive oxygen species: they can be deleterious to one cell, and, at the same time, be essential
for triggering a stress response in other cells, resulting in the complex co-evolution of antioxidative and signal transduction mechanisms. Conclusions
In spite of dealing with osmotic and oxidative stresses in a wide range of species, this conference proved highly successful on several levels. New insights have been gained from listening to lectures on two apparently distinct stress responses. At the two workshops, it became evident that the other major aim of the organizers was to stimulate new routes of communication between researchers working in different fields. The enthusiasm with which the decision to organize a follow-up meeting in 2001 (in Porto, Portugal) was met suggests that this ambition was fully realized. Heribert Hirt Vienna Biocenter, Institute of Microbiology and Genetics, Dr. Bohrgasse 9, 1030 Vienna, Austria (e-mail [email protected]) Han Asard* Dept of Biology, University of Antwerp (RUCA), Groenenborgerlaan 171, 2020 Antwerp, Belgium
*Author for correspondence (e-mail [email protected])
GM crops: environmental risks and non-target effects The debate surrounding the environmental implications of using genetically modified (GM) crops is growing increasingly complex, intense and emotional. This is complicated by the continuing twists and turns as new research is published; the conclusions of which are often misrepresented or even misinterpreted. The extensive media coverage that followed the report on monarch butterflies and transgenic plants expressing Bacillus thuringiensis (Bt) toxins1, work that has subsequently received considerable scientific criticism2 is a typical example. There have been several other notable studies addressing the ecological effect of insect- resistant GM crops on important non-target beneficial insects, such as ladybirds3, lacewings4,5 and parasitic wasps6. A recent study showed the asynchronous development of Bt-resistant and Bt-susceptible pink bollworm larvae reared in greenhouse bioassays7. Since this study, 4
January 2000, Vol. 5, No. 1
several questions have been raised concerning the use of the refugia management strategy as a means of reducing the development of resistance by lepidopteran targets on Bt crops. A central premise to the refugia management strategy is that there will be significant interbreeding between resistant and susceptible moths but that there will be little or no assortative mating within strains of moths. These scientific studies, coupled with disputes over the economic and environmental benefits of using Bt crops8,9, have intensified the debate rather than building public confidence in GM technology. The credibility of science is jeopardized when the public is not provided with the perspective and context of experiments. This could lead to science being viewed by the public as incapable of providing the credible information needed to resolve complex issues. The GM argument is multi-faceted, involving diverse issues including the non-
sustainability of modern agriculture, ethics and concern that multi-national corporations dominate the industry. Addressing all these questions is beyond the scope and length of this article, therefore I will focus on one small aspect of the current debate, namely assessing the risk of insect-resistant plants on non-target insects. Although this is only a small piece in the complex jigsaw, it is relevant to debates and discussions of GM plants in general. Bacillus thuringiensis and monarch butterflies Understanding the ecological interactions between organisms is complex and scientifically challenging. To try and fully appreciate the ecological significance of changing an abiotic or a biotic parameter requires detailed proximate and adaptive studies. This can be achieved by simplifying the system to allow individual mechanisms to be investigated. Experiments
1360 - 1385/00/$ – see front matter © 2000 Elsevier Science Ltd. All rights reserved.
trends in plant science Comment can be conducted under controlled conditions or, alternatively, by observing ‘natural’ systems, conducting manipulative experiments and using modelling to explain key factors determining the ‘natural’ system. The most logical way forward in assessing the potential environmental risk of GM crops is to adopt a tiered risk assessment, as used for evaluating the impact of insecticides on nontarget organisms10. Therefore, research begins in the laboratory by considering the so-called ‘worst-case scenario’, which is represented, often wrongly, as the ‘real’ scenario. The spatial and temporal elements should be extended to increase realism by moving to second (semi-field) tier and third (field) tier tests. This approach to risk assessment can eliminate ‘risky’ products at an early stage, and help to design and assess experiments at higher tiers. The controversial study concerning Bt pollen and monarch butterflies was a laboratory-based ‘worst-case scenario’1 that alluded to important factors concerning butterfly populations and migrations. However, these important aspects were not studied in this research paper, which was purely laboratory based. It is no surprise that monarch butterflies are susceptible to Bt toxin. One of the advantages of the Bt toxin is its apparent specificity to Lepidoptera and Coleoptera (microbial Bt sprays have been widely used by farmers, including organic farmers and beekeepers, for .40 years, with little reason for concern about effects on non-target organisms). This study raises several questions, of which two are critical. Firstly, what is the real likelihood of monarch butterflies in the field being exposed to Bt levels that are toxic to their larvae? Secondly, in cases where the influence of factors such as density dependence and insect behaviour is potentially important, can small-scale ‘worst-case scenario’ laboratory experiments based on individuals be extrapolated to the population dynamics in the field? It is possible to introduce more realism, even in small-scale laboratory studies, by allowing typical insect behaviour and choice to determine exposure and consequence6. The significance of the monarch butterfly study can only be realized following further experimentation. Moreover, the impact of Bt pollen needs to be judged against the effects of the insecticides currently used to control the European corn borer in maize fields. Direct versus indirect effects on ecological interactions
Direct versus indirect effects on ecological interactions are overlooked when assessing the potential risk of GM crops. The plant poses a direct threat to ecological interactions if the GM crop has a direct toxicological effect on populations of non-target organisms. However, if the main effect of the GM plant is to deplete populations of pest insects that are the prey of
predators or the host of parasites, then this indirect effect is a consequence of the GM plant doing its job (i.e. killing pests), and it is not a risk unique to GM technology. If the GM plant results in changes in crop management and farm practice, then the effects on farmland biodiversity might be a result of such husbandry changes rather than directly because of the GM plant. In the UK, the current farmlandscale trials using GM herbicide tolerant
“The credibility of science is jeopardized when the public is not provided with the perspective and context of experiments.” (GMHT) crops11 will address such issues by comparing the impact that those GMHT crops and conventional crops have on farmland biodiversity. Many of the criticisms being aimed directly at GM crops relate to wider questions concerning the benefits of the green revolution and of modern agricultural practice. Conceivably, the possibility of producing more crops from less land with lower inputs could reverse the trend of declining biodiversity in modern agroecosystems. Research showing that lacewing populations were affected if they ate caterpillars feeding on Bt maize3 or caterpillars fed on Bt-laced artificial diets4, has raised questions about the ecological impact of Bt plants and, more importantly, about the specificity of the Bt toxin. However, these laboratory studies were yet again ‘worst-case scenario’ experiments, conducted in a no-choice situation (i.e. only one diet was offered to the lacewings). Although most lacewings are generalist predators, their prey diet is known to influence their survival and fecundity. Confining Chrysoperla carnea lacewings (commonly known as the aphid lion) to a monophagous diet of caterpillars might have highlighted an effect observed in the laboratory on individuals that would not manifest itself in terms of the population dynamics of lacewings in the field where a choice of prey is available. In fact, data collected in fields of Bt crops in the USA have not reported detrimental effects on lacewing abundance12. However, it is difficult to compare the results directly because these studies represent different ecological communities, conducted at different scales and at different times in different countries. If a tiered risk assessment approach were to be adopted, the same research methods could be used for all the tiers and predictions, and transitions between the tiers (scales) could be made. Mick Crawley recently reiterated a well known concept to ecologists that relates well
to GM crops13, namely that taking ‘snap-shots’ of populations of organisms does not necessarily provide realistic predictions about longer term population dynamics. Therefore, predictions based on ‘snap-shots’ or, even worse, based on studies of individuals in ‘worst-case scenarios’, should be avoided. Allowing behavioural choice
A recent study involving Bt oilseed rape, the diamondback moth Plutella xylostella and a parasitic wasp Cotesia plutella is important because it illustrates how ‘snap-shots’ could lead to incorrect conclusions6. This research demonstrated that Bt did not affect the nontarget parasitic insect directly. Parasitoids did not emerge from parasitized caterpillars feeding on Bt plants because the caterpillar died before the parasitoid could develop and emerge. A strain of caterpillars resistant to Bt, and thus surviving when feeding on Bt oilseed rape, were shown to be equally suitable hosts for the parasitoid regardless of whether the caterpillars were living on GM or non-transgenic plants. This highlights the important determining factor: whether the caterpillar lives long enough for the parasitoid to develop inside it and successfully emerge. Any control measure that reduces caterpillar survival, whether cultural, conventional or organic, will also have this kind of impact on parasitic insects. This work was the first laboratory-based study to incorporate choice and allow behavioural decision making6. The first stages of successful host foraging by parasitoids involve finding where the hosts are located. In many tritrophic systems, parasitoids find their hosts by sensing the chemicals that are released from the plant when damaged by herbivore hosts14. A choice test was undertaken in a wind tunnel to assess whether transgenic plants and control plants differed in their ability to attract parasitoids. The key factor in determining whether parasitoids were attracted to caterpillar-damaged plants was the amount of damage that the caterpillar had inflicted on the plant. Bt oilseed rape did not differ in its inherent ability to attract parasitoids, but when susceptible caterpillars fed on this plant, they caused so little plant damage that the plant did not attract many parasitoids in choice tests. However, when resistant caterpillars fed on the plant and caused significant damage, these plants did attract parasitoids. These experiments demonstrate that parasitoids tend not to be attracted to dying caterpillars and prefer caterpillars that are actively damaging plants. This factor enables the Bt plant and the biocontrol agent to act in an integrated manner to eliminate the caterpillars by (i) potentially delaying the onset of problems concerning caterpillar resistance, and (ii) by parasitizing caterpillars that are able to survive on poorly expressing parts of the plant. January 2000, Vol. 5, No. 1
5
trends in plant science Comment The road ahead
Although the work on insect-resistant crops and non-target insects is only a small part of the debate concerning the environmental implications of GM technology, it encompasses many aspects of relevance to broader issues. The importance of adopting a case by case risk-assessment is imperative as different transgenes, crops and growing regimes will alter those organisms that are likely to be exposed and the possible consequences of such exposure. The complexity of assessing risk is well understood by specialists but somewhat misunderstood by non-specialists. It is an ill-informed questioner who asks about absolute safety because risk is a quantifiable measure and virtually everything we do has a risk. It is thus too simplistic to talk about the risks of GM crops without comparing their risk with that posed by conventional practices. Many scientists and policy makers refer to such benchmark comparisons, but this is a research area that deserves more attention. Many technologies pose associated economic, environmental and ethical risks that must be addressed before their benefits can be fully realized. It is important that GM crops are considered in this way, but equally important that independent assessment is allowed and that judgement is made on scientific facts rather than instinct and ‘gut-feelings’. However, we must also be aware that risk is viewed by many to 5 hazard 1 outrage. Outrage is
considered a predictable response when a community feels that it isn’t being dealt with fairly. We must be sensitive to this and try to bring trust, morality, accountability and compassion to this debate, as well as cold scientific answers. The environmental impact of GM crops must be accurately and impartially assessed so as to exploit the benefits while reducing the risks, as is currently being undertaken when assessing pesticides. The tiered risk assessment approach is the most rational way forward, but it is important to realize that laboratory studies developing ‘worst-case scenarios’ are the first part in an assessment and do not necessarily reflect the actuality of growing GM crops in the field. GM crops, including those for insect-resistance, do have a potential to disrupt ecological interactions. The purpose of risk-assessment is to halt development of such plants before field release, but only if the disruption is worse than that from conventional agricultural practice. We are just beginning to see the first generation of GM crops. The use of recombinant DNA technology in plant breeding has the potential to have a dramatic impact on food quality, product variety, environmental quality and human health. Complex decisions need to be based on facts, which are frequently being clouded in this heated debate. It is the job of scientists and the media to ensure that these facts are clearly
Important News New address for enquiries to Trends in Plant Science In January 1999, the Current Trends division of Elsevier Science London was created by bringing together the Elsevier Trends Journals, the Current Opinion Journals, Current Biology and associated publications. An important milestone in the development of this new business is the relocation of all the publications, together with BioMedNet, to a new site in central London. All communication with Trends in Plant Science should be directed to: The Editor Trends in Plant Science Elsevier Science London 84 Theobald’s Rd London UK WC1X 8RR Tel: 144 (0) 20 7611 4400 Fax: 144 (0) 20 7611 4485 E-mail: [email protected] WWW URL: http://plants.trends.com Please update all your contact databases and address books with these new details. Please note that all contact details are also available at http://www.trends.com
6
January 2000, Vol. 5, No. 1
and accurately presented, and not over-interpreted, so that the jury that matters, the public, can make an informed decision. We also need to accept that there can be degrees of acceptability, both ethically and environmentally, rather than adopt the view of the polarized camps in this debate, who appear to want acceptance of this technology on an ‘all or nothing’ basis. Acknowledgements
Thanks to Dr Jenny Baverstock for critical comments on an early draft of this paper. Thanks are also due to many colleagues who have discussed this complex topic with me over the past few years. Guy Poppy Dept of Entomology and Nematology, IACR Rothamsted, Harpenden, Herts, UK AL5 2JQ (e-mail [email protected]) References 1 Losey, J.E. et al. (1999) Transgenic pollen harms monarch larvae. Nature 399, 214 2 Hodgson, J. (1999) Monarch Bt-corn paper questioned. Nat. Biotechnol. 17, 627 3 Birch, A.N.E. et al. (1999) Tri-trophic interactions involving pest aphids, predatory 2-spot ladybirds and transgenic potatoes expressing snowdrop lectin for aphid resistance. Mol. Breed. 5, 75–83 4 Hilbeck, A. et al. (1998) Effects of transgenic Bacillus thuringiensis corn-fed prey on mortality and development time of immature Chrysoperla carnea (Nueroptera:Chrysopidae). Environ. Entomol. 27, 480–487 5 Hilbeck, A. et al. (1999) Prey-mediated effects of Cry1Ab toxin and protoxin and Cry2A protoxin on the predator Chrysopa carnea. Entomol. Exp. Appl. 91, 305–316 6 Schuler, T.H. et al. (1999) Parasitoid behaviour and Bt plants. Nature 400, 825–826 7 Liu, Y.B. et al. (1999) Development time and resistance to Bt crops. Nature 400, 519 8 Brower, V. et al. (1999). US study shows GM pros. Nat. Biotechnol. 17, 735–737 9 Reichardt, T. (1999) US send mixed message in GM debate… as questions emerge over costeffectiveness. Nature 400, 298 10 Denholm, I. et al. (1998) The complementary roles of laboratory and field testing in ecotoxicological risk assessment. In BCPC Pests and Diseases Conference (Vol. 2), pp. 583–590 11 Firbank, L. et al. (1999) Farm scale evaluation of GM crops explained. Nature 339, 727–728 12 Wilson, F.D. et al. (1992) Resistance of cotton containing a Bacillus thuringiensis toxin to pink bollworm (Lepidoptera:Gelechiidae) and other insects. J. Econ. Entomol. 85, 1516–1521 13 Crawley, M.J. (1999) Bollworms, genes and ecologists. Nature 400, 501–502 14 Poppy, G.M. (1999) The raison d’être of secondary plant chemicals. Trends Plant Sci. 4, 82–83
In contrast with the rapidly accumulating knowledge on signal transduction, relatively little is known about how cells sense oxidative or osmotic stress signals. In yeast, the Sln1 protein is involved in the perception of osmotic stress (Francesc Posas). It is com-
posed of an extracellular sensory domain and a cytoplasmic histidine kinase domain, and potentially functions as a classical ‘two component’ sensor in the induction of the HOG1 pathway. AtHK1 in Arabidopsis shows homology to Sln1, and can function as an osmosensor in yeast. At present, it is hypothesized that osmotic stress-induced cell size changes might exert increased lateral pressure on the membrane-spanning osmosensors, and thereby bring about conformational changes and activation of the kinases. Thought provoking questions
Two workshop sessions were organized to promote the exchange of ideas and viewpoints between researchers from the different fields. Although it is often difficult to animate group sessions, the discussion leaders Dennis Thiele (University of Michigan, USA) and Stefan Hohmann provided several thought provoking questions. For example, the question was raised, whether induction of a certain set of stress genes might also lead to cross protection against other stresses. To date, only a few results point in this direction, therefore this question requires further investigations before it can be answered. The discussion also emphasized the dual function of reactive oxygen species: they can be deleterious to one cell, and, at the same time, be essential
for triggering a stress response in other cells, resulting in the complex co-evolution of antioxidative and signal transduction mechanisms. Conclusions
In spite of dealing with osmotic and oxidative stresses in a wide range of species, this conference proved highly successful on several levels. New insights have been gained from listening to lectures on two apparently distinct stress responses. At the two workshops, it became evident that the other major aim of the organizers was to stimulate new routes of communication between researchers working in different fields. The enthusiasm with which the decision to organize a follow-up meeting in 2001 (in Porto, Portugal) was met suggests that this ambition was fully realized. Heribert Hirt Vienna Biocenter, Institute of Microbiology and Genetics, Dr. Bohrgasse 9, 1030 Vienna, Austria (e-mail [email protected]) Han Asard* Dept of Biology, University of Antwerp (RUCA), Groenenborgerlaan 171, 2020 Antwerp, Belgium
*Author for correspondence (e-mail [email protected])
GM crops: environmental risks and non-target effects The debate surrounding the environmental implications of using genetically modified (GM) crops is growing increasingly complex, intense and emotional. This is complicated by the continuing twists and turns as new research is published; the conclusions of which are often misrepresented or even misinterpreted. The extensive media coverage that followed the report on monarch butterflies and transgenic plants expressing Bacillus thuringiensis (Bt) toxins1, work that has subsequently received considerable scientific criticism2 is a typical example. There have been several other notable studies addressing the ecological effect of insect- resistant GM crops on important non-target beneficial insects, such as ladybirds3, lacewings4,5 and parasitic wasps6. A recent study showed the asynchronous development of Bt-resistant and Bt-susceptible pink bollworm larvae reared in greenhouse bioassays7. Since this study, 4
January 2000, Vol. 5, No. 1
several questions have been raised concerning the use of the refugia management strategy as a means of reducing the development of resistance by lepidopteran targets on Bt crops. A central premise to the refugia management strategy is that there will be significant interbreeding between resistant and susceptible moths but that there will be little or no assortative mating within strains of moths. These scientific studies, coupled with disputes over the economic and environmental benefits of using Bt crops8,9, have intensified the debate rather than building public confidence in GM technology. The credibility of science is jeopardized when the public is not provided with the perspective and context of experiments. This could lead to science being viewed by the public as incapable of providing the credible information needed to resolve complex issues. The GM argument is multi-faceted, involving diverse issues including the non-
sustainability of modern agriculture, ethics and concern that multi-national corporations dominate the industry. Addressing all these questions is beyond the scope and length of this article, therefore I will focus on one small aspect of the current debate, namely assessing the risk of insect-resistant plants on non-target insects. Although this is only a small piece in the complex jigsaw, it is relevant to debates and discussions of GM plants in general. Bacillus thuringiensis and monarch butterflies Understanding the ecological interactions between organisms is complex and scientifically challenging. To try and fully appreciate the ecological significance of changing an abiotic or a biotic parameter requires detailed proximate and adaptive studies. This can be achieved by simplifying the system to allow individual mechanisms to be investigated. Experiments
1360 - 1385/00/$ – see front matter © 2000 Elsevier Science Ltd. All rights reserved.
trends in plant science Comment can be conducted under controlled conditions or, alternatively, by observing ‘natural’ systems, conducting manipulative experiments and using modelling to explain key factors determining the ‘natural’ system. The most logical way forward in assessing the potential environmental risk of GM crops is to adopt a tiered risk assessment, as used for evaluating the impact of insecticides on nontarget organisms10. Therefore, research begins in the laboratory by considering the so-called ‘worst-case scenario’, which is represented, often wrongly, as the ‘real’ scenario. The spatial and temporal elements should be extended to increase realism by moving to second (semi-field) tier and third (field) tier tests. This approach to risk assessment can eliminate ‘risky’ products at an early stage, and help to design and assess experiments at higher tiers. The controversial study concerning Bt pollen and monarch butterflies was a laboratory-based ‘worst-case scenario’1 that alluded to important factors concerning butterfly populations and migrations. However, these important aspects were not studied in this research paper, which was purely laboratory based. It is no surprise that monarch butterflies are susceptible to Bt toxin. One of the advantages of the Bt toxin is its apparent specificity to Lepidoptera and Coleoptera (microbial Bt sprays have been widely used by farmers, including organic farmers and beekeepers, for .40 years, with little reason for concern about effects on non-target organisms). This study raises several questions, of which two are critical. Firstly, what is the real likelihood of monarch butterflies in the field being exposed to Bt levels that are toxic to their larvae? Secondly, in cases where the influence of factors such as density dependence and insect behaviour is potentially important, can small-scale ‘worst-case scenario’ laboratory experiments based on individuals be extrapolated to the population dynamics in the field? It is possible to introduce more realism, even in small-scale laboratory studies, by allowing typical insect behaviour and choice to determine exposure and consequence6. The significance of the monarch butterfly study can only be realized following further experimentation. Moreover, the impact of Bt pollen needs to be judged against the effects of the insecticides currently used to control the European corn borer in maize fields. Direct versus indirect effects on ecological interactions
Direct versus indirect effects on ecological interactions are overlooked when assessing the potential risk of GM crops. The plant poses a direct threat to ecological interactions if the GM crop has a direct toxicological effect on populations of non-target organisms. However, if the main effect of the GM plant is to deplete populations of pest insects that are the prey of
predators or the host of parasites, then this indirect effect is a consequence of the GM plant doing its job (i.e. killing pests), and it is not a risk unique to GM technology. If the GM plant results in changes in crop management and farm practice, then the effects on farmland biodiversity might be a result of such husbandry changes rather than directly because of the GM plant. In the UK, the current farmlandscale trials using GM herbicide tolerant
“The credibility of science is jeopardized when the public is not provided with the perspective and context of experiments.” (GMHT) crops11 will address such issues by comparing the impact that those GMHT crops and conventional crops have on farmland biodiversity. Many of the criticisms being aimed directly at GM crops relate to wider questions concerning the benefits of the green revolution and of modern agricultural practice. Conceivably, the possibility of producing more crops from less land with lower inputs could reverse the trend of declining biodiversity in modern agroecosystems. Research showing that lacewing populations were affected if they ate caterpillars feeding on Bt maize3 or caterpillars fed on Bt-laced artificial diets4, has raised questions about the ecological impact of Bt plants and, more importantly, about the specificity of the Bt toxin. However, these laboratory studies were yet again ‘worst-case scenario’ experiments, conducted in a no-choice situation (i.e. only one diet was offered to the lacewings). Although most lacewings are generalist predators, their prey diet is known to influence their survival and fecundity. Confining Chrysoperla carnea lacewings (commonly known as the aphid lion) to a monophagous diet of caterpillars might have highlighted an effect observed in the laboratory on individuals that would not manifest itself in terms of the population dynamics of lacewings in the field where a choice of prey is available. In fact, data collected in fields of Bt crops in the USA have not reported detrimental effects on lacewing abundance12. However, it is difficult to compare the results directly because these studies represent different ecological communities, conducted at different scales and at different times in different countries. If a tiered risk assessment approach were to be adopted, the same research methods could be used for all the tiers and predictions, and transitions between the tiers (scales) could be made. Mick Crawley recently reiterated a well known concept to ecologists that relates well
to GM crops13, namely that taking ‘snap-shots’ of populations of organisms does not necessarily provide realistic predictions about longer term population dynamics. Therefore, predictions based on ‘snap-shots’ or, even worse, based on studies of individuals in ‘worst-case scenarios’, should be avoided. Allowing behavioural choice
A recent study involving Bt oilseed rape, the diamondback moth Plutella xylostella and a parasitic wasp Cotesia plutella is important because it illustrates how ‘snap-shots’ could lead to incorrect conclusions6. This research demonstrated that Bt did not affect the nontarget parasitic insect directly. Parasitoids did not emerge from parasitized caterpillars feeding on Bt plants because the caterpillar died before the parasitoid could develop and emerge. A strain of caterpillars resistant to Bt, and thus surviving when feeding on Bt oilseed rape, were shown to be equally suitable hosts for the parasitoid regardless of whether the caterpillars were living on GM or non-transgenic plants. This highlights the important determining factor: whether the caterpillar lives long enough for the parasitoid to develop inside it and successfully emerge. Any control measure that reduces caterpillar survival, whether cultural, conventional or organic, will also have this kind of impact on parasitic insects. This work was the first laboratory-based study to incorporate choice and allow behavioural decision making6. The first stages of successful host foraging by parasitoids involve finding where the hosts are located. In many tritrophic systems, parasitoids find their hosts by sensing the chemicals that are released from the plant when damaged by herbivore hosts14. A choice test was undertaken in a wind tunnel to assess whether transgenic plants and control plants differed in their ability to attract parasitoids. The key factor in determining whether parasitoids were attracted to caterpillar-damaged plants was the amount of damage that the caterpillar had inflicted on the plant. Bt oilseed rape did not differ in its inherent ability to attract parasitoids, but when susceptible caterpillars fed on this plant, they caused so little plant damage that the plant did not attract many parasitoids in choice tests. However, when resistant caterpillars fed on the plant and caused significant damage, these plants did attract parasitoids. These experiments demonstrate that parasitoids tend not to be attracted to dying caterpillars and prefer caterpillars that are actively damaging plants. This factor enables the Bt plant and the biocontrol agent to act in an integrated manner to eliminate the caterpillars by (i) potentially delaying the onset of problems concerning caterpillar resistance, and (ii) by parasitizing caterpillars that are able to survive on poorly expressing parts of the plant. January 2000, Vol. 5, No. 1
5
trends in plant science Comment The road ahead
Although the work on insect-resistant crops and non-target insects is only a small part of the debate concerning the environmental implications of GM technology, it encompasses many aspects of relevance to broader issues. The importance of adopting a case by case risk-assessment is imperative as different transgenes, crops and growing regimes will alter those organisms that are likely to be exposed and the possible consequences of such exposure. The complexity of assessing risk is well understood by specialists but somewhat misunderstood by non-specialists. It is an ill-informed questioner who asks about absolute safety because risk is a quantifiable measure and virtually everything we do has a risk. It is thus too simplistic to talk about the risks of GM crops without comparing their risk with that posed by conventional practices. Many scientists and policy makers refer to such benchmark comparisons, but this is a research area that deserves more attention. Many technologies pose associated economic, environmental and ethical risks that must be addressed before their benefits can be fully realized. It is important that GM crops are considered in this way, but equally important that independent assessment is allowed and that judgement is made on scientific facts rather than instinct and ‘gut-feelings’. However, we must also be aware that risk is viewed by many to 5 hazard 1 outrage. Outrage is
considered a predictable response when a community feels that it isn’t being dealt with fairly. We must be sensitive to this and try to bring trust, morality, accountability and compassion to this debate, as well as cold scientific answers. The environmental impact of GM crops must be accurately and impartially assessed so as to exploit the benefits while reducing the risks, as is currently being undertaken when assessing pesticides. The tiered risk assessment approach is the most rational way forward, but it is important to realize that laboratory studies developing ‘worst-case scenarios’ are the first part in an assessment and do not necessarily reflect the actuality of growing GM crops in the field. GM crops, including those for insect-resistance, do have a potential to disrupt ecological interactions. The purpose of risk-assessment is to halt development of such plants before field release, but only if the disruption is worse than that from conventional agricultural practice. We are just beginning to see the first generation of GM crops. The use of recombinant DNA technology in plant breeding has the potential to have a dramatic impact on food quality, product variety, environmental quality and human health. Complex decisions need to be based on facts, which are frequently being clouded in this heated debate. It is the job of scientists and the media to ensure that these facts are clearly
Important News New address for enquiries to Trends in Plant Science In January 1999, the Current Trends division of Elsevier Science London was created by bringing together the Elsevier Trends Journals, the Current Opinion Journals, Current Biology and associated publications. An important milestone in the development of this new business is the relocation of all the publications, together with BioMedNet, to a new site in central London. All communication with Trends in Plant Science should be directed to: The Editor Trends in Plant Science Elsevier Science London 84 Theobald’s Rd London UK WC1X 8RR Tel: 144 (0) 20 7611 4400 Fax: 144 (0) 20 7611 4485 E-mail: [email protected] WWW URL: http://plants.trends.com Please update all your contact databases and address books with these new details. Please note that all contact details are also available at http://www.trends.com
6
January 2000, Vol. 5, No. 1
and accurately presented, and not over-interpreted, so that the jury that matters, the public, can make an informed decision. We also need to accept that there can be degrees of acceptability, both ethically and environmentally, rather than adopt the view of the polarized camps in this debate, who appear to want acceptance of this technology on an ‘all or nothing’ basis. Acknowledgements
Thanks to Dr Jenny Baverstock for critical comments on an early draft of this paper. Thanks are also due to many colleagues who have discussed this complex topic with me over the past few years. Guy Poppy Dept of Entomology and Nematology, IACR Rothamsted, Harpenden, Herts, UK AL5 2JQ (e-mail [email protected]) References 1 Losey, J.E. et al. (1999) Transgenic pollen harms monarch larvae. Nature 399, 214 2 Hodgson, J. (1999) Monarch Bt-corn paper questioned. Nat. Biotechnol. 17, 627 3 Birch, A.N.E. et al. (1999) Tri-trophic interactions involving pest aphids, predatory 2-spot ladybirds and transgenic potatoes expressing snowdrop lectin for aphid resistance. Mol. Breed. 5, 75–83 4 Hilbeck, A. et al. (1998) Effects of transgenic Bacillus thuringiensis corn-fed prey on mortality and development time of immature Chrysoperla carnea (Nueroptera:Chrysopidae). Environ. Entomol. 27, 480–487 5 Hilbeck, A. et al. (1999) Prey-mediated effects of Cry1Ab toxin and protoxin and Cry2A protoxin on the predator Chrysopa carnea. Entomol. Exp. Appl. 91, 305–316 6 Schuler, T.H. et al. (1999) Parasitoid behaviour and Bt plants. Nature 400, 825–826 7 Liu, Y.B. et al. (1999) Development time and resistance to Bt crops. Nature 400, 519 8 Brower, V. et al. (1999). US study shows GM pros. Nat. Biotechnol. 17, 735–737 9 Reichardt, T. (1999) US send mixed message in GM debate… as questions emerge over costeffectiveness. Nature 400, 298 10 Denholm, I. et al. (1998) The complementary roles of laboratory and field testing in ecotoxicological risk assessment. In BCPC Pests and Diseases Conference (Vol. 2), pp. 583–590 11 Firbank, L. et al. (1999) Farm scale evaluation of GM crops explained. Nature 339, 727–728 12 Wilson, F.D. et al. (1992) Resistance of cotton containing a Bacillus thuringiensis toxin to pink bollworm (Lepidoptera:Gelechiidae) and other insects. J. Econ. Entomol. 85, 1516–1521 13 Crawley, M.J. (1999) Bollworms, genes and ecologists. Nature 400, 501–502 14 Poppy, G.M. (1999) The raison d’être of secondary plant chemicals. Trends Plant Sci. 4, 82–83