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This file was created by scanning the printed publication. Errors identified by the software have been corrected; however, some errors may remain. Chapter32 Environmental Risk Assesslnent and Deployment Strategies for Genetically Engineered Insect-Resistant Populus1 Kenneth F. Raffa, Karl W. Kleiner, David D. Ellis, and Brent H. McCown chapter, environmental risk means: "the likelihood that Introduction release of a novel material will cause adverse effects such as mortality or reduction in populations of nontarget or­ ganisms due to acute, chronic, or reproductive effects, or Most studies on genetically engineered plants have con­ disruption of community or ecosystem function" {Urban centrated on efficacy; few have focused on environmental and Cook 1986). Predicting consequences becomes increas­ safety {Seidler and Levin 1994). This emphasis reflects the ingly complex as the scale expands from individual- to rapid increase in our technological capabilities over the last community-level interactions. For example, negative effects 15 years and reflects an uncertainty over how best to scien­ on individuals do not necessarily translate into reduced tifically generate relative rankings of the likelihood and se­ populations. Natural and managed systems provide many verity of possible adverse effects. Environmental risk instances of compensatory feedback where removing assessment is not an exact science and can only provide di­ substantial numbers of individuals does not affect popu­ rect comparisons between treatments and checks under the lation density. Conversely, the prospect of indirect effects most controlled, and therefore least realistic, conditions. from community-level interactions, even when no indi­ Moreover, risk assessment inevitably raises questions that vidual effects appear important, is a serious concern. Ba­ are at least partially subjective, value-laden, and contextual. sic ecological studies provide a wealth of examples. This chapter attempts to ·identify the more significant Indirect interactions, across multiple trophic levels, incor­ issues of environmental risk, weigh their relative impacts, porating biotic and abiotic environmental factors, and and suggest possible strategies for reducing adverse ef­ mediated by a broad range of symbionts, competitors, and fects. We limit our discussion to potential environmental alternate hosts, can exert enormous influences and gen­ effects. Impacts on social and economic systems, while erate unpredicted outcomes {Angle 1994; Bergelson 1994; important, are beyond our expertise. Ehler 1990; Holt 1977; Price et al. 1980; Simberloff 1985). Similarly, the history of applied ecologies, such as agri­ culture and forestry, shows that indirect interactions of­ ten yield the least predictable yet most damaging consequences. Approaches to Environmental The issue of ecological complexity is a paradox to risk Risk Assessment assessment. Controlled evaluations of acute effects on iso­ lated individuals generate the least variable and seemingly most "reliable" results. Studies that attempt to unravel An appropriate definition of environmental risk is de­ more diffuse and incipient effects are ultimately more im­ batable (Morgan 1993; Wilson and Crouch 1987). In this portant, yet unfortunately they are less likely to provide definitive answers {Angle 1994). Ironically, current ap­ proaches to training, funding, and productivity are strongly biased toward the former approach. Comprehensive risk assessment must also weigh antici­ 1 Klopfenstein, N.B.; Chun, Y. W.; Kim, M.-S.; Ahuja, M.A., eds. pated benefits against risk. Genetic engineering of Populus Dillon, M.C.; Carman. R.C.; Eskew. L.G., tech. eds. 1997. Micropropagation. genetic engineering. and molecular biology offers several potential benefits, such as reduced pesticidal of Populus. Gen. Tech. Rep. RM-GTR-297. Fort Collins, CO: inputs, improved carbon sequestration, alleviation of pres­ U.S. Department of Agriculture, Forest Service, Rocky Mountain sures to exploit unmanaged systems, and improved Research Station. 326 p. sources of alternatives to fossil fuels {Kleiner et al. 1995; 249 Section V Biotechnological Applications McCown et al. 1991; Raffa 1989; Raffa et al. 1993; Robison systems. Molecular expertise is invaluable, however, in et al. 1994). These are potentially enormous benefits; how­ protecting against unintended changes in the genome, in­ ever, they are beyond the scope of this paper. corporating methods of sterility, and controlling and evalu­ Potential risks can be categorized based on their spatial ating patterns of expression. The criteria for estimating and and temporal scales. For example, an effect could be lim­ the approaches to alleviating environmental concerns re­ ited to the treated site, or it could impact neighboring eco­ quire interdisciplinary efforts (Raffa 1989). systems. Effects can be short-term, such as the release of a Raising every imaginable hazard that could arise from toxic gene product into the environment, or self-replicat­ genetically engineered organisms is neither difficult nor ing, such as the escape of viable germplasm. Such distinc­ helpful. This approach could hinder the enormous value tions can be somewhat blurred and need to be assessed as of biotechnology and dilute needed emphasis on legiti­ part of the complete risk evaluation process. Still, there is mate concerns. At the other extreme, the view is some­ general agreement that the most serious concerns arise times expressed (or implied) that all concerns arise merely when genetically engineered organisms could cause self­ from a lack of scientific understanding or breadth. This perpetuating injury to commercial or natural ecosystems view seriously underestimates the complexity of scaling beyond the immediate area of release. from molecular- through ecosystem- level processes. Fail­ ure to consider such complexity invariably detracts from the long-term sustainability of new technologies; a costly lesson already appreciated by agrichemical companies. The issue needs to be one of reasonable probability (de Zoeten Criteria for Risk Assessment 1991; Frederick and Egan 1994; Hubbes 1993; NAS 1989; Raffa 1989; Strauss et al. 1991; Tiedje et al. 1989). For ex­ Different individuals, agencies, and organizations have ample, Tolin and Vidaver (1989) propose that "restrictions advocated different criteria, burdens of proof, and levels should be based on demonstrated, not conjectural risks." of evidence governing the planned release of genetically However, we would substitute "realistic" for "demon­ engineered organisms. Probably the most helpful guidance strated" to promote a more proactive approach· to risk is provided by a National Academy of Sciences commit­ management. In our view, the likelihood of risk may be tee headed by Arthur Kelman (NAS 1987). In the opinion realistic if 2 conditions are met: 1) a clear mechanism, based of NAS, what matters is the product not the process. Ac­ on known biological processes and verified assumptions, cording to this perspective, introducing genetically engi­ can be delineated; and 2) there is relevant precedent. neered organisms "poses no risks different from the Few specific risks meet the above criteria. Those that do introduction of unmodified organisms and organisms can be classified into 3 general categories: 1) escaped plants modified by other methods." Therefore, "assessment of risk or genes, 2) evolution and consequences of resistant pest should be based on the organism, not the method of engi­ biotypes, and 3) alteration of multi-trophic processes. We neering." Subsequent authors have delineated some im­ first describe how Populus systems relate to these ques­ portant differences between g~netic engineering and plant tions and then address each risk. Biotype evolution will breeding, and hence the need for limits in applying this be developed as a more detailed case study, as this is our equivalency (Dale and Irwin 1995; Giampietro 1994; Re­ primary area of interest. We conclude with an overall syn­ gal 1994). However, this starting point has proven useful thesis of environmental risk assessment in Populus. and has withstood the test of time. Similar conclusions are For each concern, the potential risk can be addressed stated by Tiedje et al. (1989) in an Ecological Society of by asking 3 questions: 1) "Is there assurance that the pro­ America report: "transgenic organisms should be evalu­ posed event (i.e., gene escape, biotype evolution, altered ated and regulated according to their biological proper­ multi-trophic process) will not occur?"; 2) "Is there assur­ ties (phenotypes), rather than according to the genetic ance that the effects will be harmless if this event does techniques used to produce them." occur?"; and 3) "Are there ways for reducing the likeli­ Emphasizing phenotypes over the methods by which hood and impact of harmful effects?" These questions they arise has proven useful because it rebuts scientifically place the burden of proof on the novel gene product to be unfounded criticisms and focuses on interactions between consistent with ~ow other novel products such as biologi­ gene products and their environment. Rather than dismiss­ cal control agents, introduced plant materials, and pesti­ ing environmental concerns, this approach highlights the cides are evaluated (Caltagirone and Huffaker 1980; importance and complexity of predicting responses to gene Charudattan and Browning 1992; FIFRA 1978; Fuester products at the community level, and the need for eco­ 1993;

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