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• W1970542021 abstract "Although public opinion is important in deciding what is valued by society, governments have determined that scientific expertise is required to evaluate potential environmental effects of genetically modified (GM) crops. We suggest how to evaluate rigorously the environmental effects of GM crops in the context of a scientific investigation. Following a disciplined scientific approach to environmental risk assessment (ERA) for GM crops should help resolve controversy in identifying and addressing risk. Although public opinion is important in deciding what is valued by society, governments have determined that scientific expertise is required to evaluate potential environmental effects of genetically modified (GM) crops. We suggest how to evaluate rigorously the environmental effects of GM crops in the context of a scientific investigation. Following a disciplined scientific approach to environmental risk assessment (ERA) for GM crops should help resolve controversy in identifying and addressing risk. Government regulation of GM crops (or other agricultural technologies) is designed to serve society. As such, societal concerns and values are captured in regulatory policy. Protection of the environment is one objective of such policy. Although public opinion is important in determining what is valued by society (i.e., what should be protected), regulators with scientific expertise evaluate specific technologies for their effects on the environment in the context of what is valued and is to be protected. Governments have universally determined that scientific expertise is required to evaluate the potential for environmental effects of new agricultural technologies such as GM crops, and that public opinion for or against a specific technology is not necessarily a good measure for what will benefit society. The majority of citizens do not have the training, time, or expertise to sort out facts from misinformation, so dedicated teams of trained regulatory scientists conduct these evaluations to ensure that the technologies that are brought forward to address the challenges of agricultural production do not pose unreasonable risk [1Romeis J. et al.When bad science makes good headlines: Bt maize and regulatory bans.Nat. Biotechnol. 2013; 31: 386-387Crossref PubMed Scopus (58) Google Scholar]. Here, we suggest how to evaluate rigorously the environmental effects of GM crops in the context of a scientific investigation. A key element of an ecological or ERA for agricultural practices is deciding what constitutes a harmful effect. In ERA jargon, this is often predicated on identifying protection goals (e.g., which species or ecological functions are to be protected). Although this concept may seem straightforward and logical to many, this step in the ERA process is actually controversial in some circles [2Herman R.A. Raybould A. Invoking ideology in the promotion of ecological risk assessment for GM crops.Trends Biotechnol. 2013; 31: 217-218Abstract Full Text Full Text PDF PubMed Scopus (6) Google Scholar]. An alternative approach is to measure an array of endpoints (typically counts of individuals within species that show up) in field studies, and then decide if results support environmental safety. Here, we discuss the former approach to ERA for GM crops based on identified protection goals. This approach follows the traditional scientific method of hypothesis formulation followed by experimental testing. Whether we choose to protect certain species or ecological functions depends on our values. When our activities affect only ourselves as individuals, our own values may be the sole determinant of what should be protected. When effects of activities are spread widely, we require a collective set of values. For the risks of agricultural practices, collective values may be expressed as the objectives of agricultural and environmental policy, and these objectives are the basis of protection goals for regulatory risk assessments. In identifying regulatory protection goals, the intentions of relevant policies must be interpreted [3Sanvido O. et al.Evaluating environmental risks of genetically modified crops: ecological harm criteria for regulatory decision-making.Environ. Sci. Policy. 2012; 15: 82-91Crossref Scopus (95) Google Scholar]. The objectives of policy are often broad; for example, protecting biodiversity or increasing agricultural production. From these broad objectives, specific attributes of the environment that will be the focus of the risk assessment must be identified. These attributes might be the abundance of particular species or the provision of an ecological function, such as pollination. Deriving unambiguous and measurable environmental attributes from broad policy objectives is called making the protection goals operational (Box 1).Box 1Making protection goals operationalOperational protection goals: A key step in bringing effective scientific discipline to ecological risk assessment is the development of operational protection goals. This is done by translating a loosely defined policy protection goal such as ‘protect biodiversity’ into relevant and measurable outcomes. There are three steps in the translation: establishing value, understanding context, and defining the endpoint. An example of a value is an important biological function where disruption would cause long-term harm. The context describes the protection boundaries. Spatial context defines the area to be protected – within a field, a field edge, or a region. Temporal context defines the time element for protection – a short interval within a growing season versus effects lasting beyond a growing season. Taxonomic or functional boundaries define the assessment level – populations, communities, or ecosystems. Once the value and context are defined, then finally the endpoint can be linked to the value and defined as a hypothesis: a species population critical to providing a valued function will not be adversely affected in a certain way over a specified space and time.Endpoint selection: High quality regulatory decisions can only be made when hypotheses are constructed such that experiments can be designed to measure changes in appropriate endpoints.Useful questions to ask when selecting endpoints include:(i)Can it be measured and is the endpoint useful in making decisions regarding harm? Not all things that can be measured and tested statistically are of equal value in determining the potential for biological significance that might indicate the potential for future harm.(ii)Is what is being measured representative of the temporal and spatial area requiring protection? A short-term depression in a population of a globally distributed highly mobile insect with short recovery time within a single agricultural field would have a lower level of biological significance compared with a regional population decrease of the same magnitude in a longer-lived organism restricted to a small geographic area.(iii)Does the endpoint represent a valued function in the ecosystem (or in the case of charismatic species, a value to society)? Although all species have value, most ecosystem functions may be carried out by numerous different species. It is highly unlikely that decreases in populations of a single species within a field will have any biologically significant effect on ecosystem function; especially when viewed within the broader context of the potential effects of agricultural practices on the environment. Operational protection goals: A key step in bringing effective scientific discipline to ecological risk assessment is the development of operational protection goals. This is done by translating a loosely defined policy protection goal such as ‘protect biodiversity’ into relevant and measurable outcomes. There are three steps in the translation: establishing value, understanding context, and defining the endpoint. An example of a value is an important biological function where disruption would cause long-term harm. The context describes the protection boundaries. Spatial context defines the area to be protected – within a field, a field edge, or a region. Temporal context defines the time element for protection – a short interval within a growing season versus effects lasting beyond a growing season. Taxonomic or functional boundaries define the assessment level – populations, communities, or ecosystems. Once the value and context are defined, then finally the endpoint can be linked to the value and defined as a hypothesis: a species population critical to providing a valued function will not be adversely affected in a certain way over a specified space and time. Endpoint selection: High quality regulatory decisions can only be made when hypotheses are constructed such that experiments can be designed to measure changes in appropriate endpoints. Useful questions to ask when selecting endpoints include:(i)Can it be measured and is the endpoint useful in making decisions regarding harm? Not all things that can be measured and tested statistically are of equal value in determining the potential for biological significance that might indicate the potential for future harm.(ii)Is what is being measured representative of the temporal and spatial area requiring protection? A short-term depression in a population of a globally distributed highly mobile insect with short recovery time within a single agricultural field would have a lower level of biological significance compared with a regional population decrease of the same magnitude in a longer-lived organism restricted to a small geographic area.(iii)Does the endpoint represent a valued function in the ecosystem (or in the case of charismatic species, a value to society)? Although all species have value, most ecosystem functions may be carried out by numerous different species. It is highly unlikely that decreases in populations of a single species within a field will have any biologically significant effect on ecosystem function; especially when viewed within the broader context of the potential effects of agricultural practices on the environment. To begin derivation of operational protection goals, organisms may be grouped into beneficial species and charismatic species. Beneficial species often include biocontrol agents that are valuable in controlling agricultural pests (e.g., predatory insects such as lady beetles). Beneficial species may also include species that serve more than agriculture, such as bats that eat biting mosquitoes. Charismatic species may include iconic species such as monarch butterflies, which provide beauty to the environment. In addition to individual species, goals may involve protecting environmental function such as soil fertility, where beneficial microbes and earthworms might be important. Finally, species richness or biodiversity may be a protection goal in which the number of species or taxa rather than the number of individuals or their environmental function may be the focus [4Carpenter J.E. Impact of GM crops on biodiversity.GM Crops. 2011; 2: 7-23Crossref PubMed Scopus (73) Google Scholar]. Biodiversity is often seen as a measure of environmental stability and as a natural resource, and may also be of aesthetic value [5Mace G.M. et al.Biodiversity and ecosystem services: a multilayered relationship.Trends Ecol. Evol. 2012; 27: 19-26Abstract Full Text Full Text PDF PubMed Scopus (1101) Google Scholar]. It is important to distinguish the aforementioned operational protection goals from vague goals like protecting the environment that often lead to experiments without clear hypotheses addressing the likelihood of harmful effects, resulting in data with dubious value in an ERA. One should be able to identify with some reasonable level of specificity what is desirable to protect and why, before experiments intended to support risk assessment are conducted and data are collected. In this way, interpretation of the data can be directed toward evaluating the impact of any observed effect on what is desirable to protect. Without this scientific discipline, experiments are descriptive rather than tests of hypotheses relevant to risk. An additional aspect of defining protection goals is a consideration of whether effects are spatially and temporally restricted to the agricultural field where the GM crop is grown, or whether the effects extend beyond the field margins and cropping cycle. A localized effect might be an impact on a population of relatively immobile predatory insects, which is reduced due to an insecticidal trait that significantly reduces a pest that is a primary food item for the biocontrol agent. The former is an indirect effect, but it is also possible for an insecticidal trait to have a direct adverse effect on a beneficial species. For example, if an insecticidal trait is directly toxic to a beneficial insect species and it is present in pollen, species that eat pollen (e.g., some lady beetle species) could be directly affected. Direct and indirect effects beyond field margins are also possible. If an herbicide tolerance trait allows farmers to obtain higher levels of weed control in their crop compared with other methods, less weed seed may be available for species that eat this seed (e.g., some birds). If the greater landscape cannot adequately support populations of these highly mobile bird species, then the agricultural practice will adversely affect populations [6Watkinson A.R. et al.Predictions of biodiversity response to genetically modified herbicide-tolerant crops.Science. 2000; 289: 1554-1557Crossref PubMed Scopus (171) Google Scholar]. As with in-field effects, it is also possible for there to be direct toxicity to highly mobile species and such effects should also be considered. It is noteworthy that landscape level benefits from GM crops are also possible such as reduced soil erosion through greater adoption of conservation tillage using herbicide-tolerant crops, and increased populations of beneficial insects, on a landscape scale, where insect-tolerant crops have replaced broad-spectrum insecticides [4Carpenter J.E. Impact of GM crops on biodiversity.GM Crops. 2011; 2: 7-23Crossref PubMed Scopus (73) Google Scholar, 7Lu Y. et al.Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services.Nature. 2012; 487: 362-365Crossref PubMed Scopus (633) Google Scholar]. Farmers have experience balancing in-field direct effects of agricultural practices such as the use of broad-spectrum pesticides which may kill both pests and beneficial arthropods. For example, use of pyrethroid insecticides to manage pests is known to increase pest mite populations in apple orchards due to predator reduction [8Hall F.R. Effects of synthetic pyrethroids on major insect and mite pests of apple.J. Econ. Entomol. 1979; 72: 441-446Google Scholar]. Farmers need to balance this negative effect with the benefits of using these products. If the effects of an agricultural practice are restricted to the farmer's field, it would seem that market pressures will address the cost–benefit ratio of the practice. Of course, farmers should be made aware of any known downsides to the use of a product as well as its benefits, but if they are aware of the trade-offs, it would seem that the farmers will incur the benefits and risks, and thus the decision to use the technology, or not, should rest with them. If they do not see a net benefit, they will not continue to use the technology. A similar scenario occurs when populations of relatively immobile predators are reduced due to fewer pests in a field on which the predators can feed. In this case, the ecological function of biological pest control may be reduced and the farmer will need to weigh this loss of function against the benefit of the reduced pest population due to use of an insecticidal trait. Ultimately, this will be driven by costs of production. GM crops are not unique in causing potential ecological effects, so existing literature should be useful in understanding the spatial localization of many effects that could be caused by these crops. For effects that extend outside of the field, the risks (and benefits) may be shared by others besides the farmer using the practice, so government regulation is often used to address these risks equitably. Direct effects, such as toxicity to a highly mobile and beneficial species (e.g., pollinating honey bees), represents a straightforward example. Again, a pesticidal case provides a clear path to a solution for addressing the concerns of multiple stakeholders. For broad-spectrum insecticides toxic to honey bees, applications may be restricted during the bloom period (when bees are attracted to the crop), thus limiting exposure [9Riedl H. et al.How to reduce bee poisoning from pesticides. Extension publication, Oregon State University, 2006http://scholarsarchive.library.oregonstate.edu/xmlui/bitstream/handle/1957/20772/pnw591.pdf?sequence=1Google Scholar]. Similarly, programs are often in place to lessen soil erosion and fertilizer run-off that could affect waterways (e.g., sediment control practices) [10Rao M. et al.A web-based GIS Decision Support System for managing and planning USDA's Conservation Reserve Program (CRP).Environ. Model. Software. 2007; 22: 1270-1280Crossref Scopus (97) Google Scholar]. Actions to address indirect effects that extend outside of a farmer's field are less universally accepted or applied. A classic example is the case of herbicide-tolerant crops that often allow high levels of weed control within agricultural fields (analogous to using highly effective herbicides on non-GM crops). This can adversely affect populations of birds that feed on weed seeds [4Carpenter J.E. Impact of GM crops on biodiversity.GM Crops. 2011; 2: 7-23Crossref PubMed Scopus (73) Google Scholar, 7Lu Y. et al.Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services.Nature. 2012; 487: 362-365Crossref PubMed Scopus (633) Google Scholar]. Two approaches have been adopted by different government regulatory agencies. In the US, farmers are given incentives to set aside land specifically for wildlife, whereas in some European countries, farmers may be restricted from using highly effective weed control measures so that some weeds will grow in their agricultural fields [11Herman R.A. Ecological risk assessment for transgenic crops: separating the seed from the chaff.Trends Biotechnol. 2010; 28: 159-160Abstract Full Text Full Text PDF PubMed Scopus (1) Google Scholar]. Although one can advocate either approach in the absence of objective data, this controversy can be informed by clearly defining protection goals and designing experiments to determine the efficiency of each approach. Based on the crop, environment, and protection goals, it should be straightforward to compare experimentally the loss of agricultural production efficiency due to inferior weed control within agricultural production areas with the production loss due to setting aside dedicated wildlife land that provides the same level of benefit to the environment. As such, alternative approaches with equivalent benefits could be presented as options for mitigating adverse effects. An additional concept that is important to consider when addressing protection goals is the context of agriculture [4Carpenter J.E. Impact of GM crops on biodiversity.GM Crops. 2011; 2: 7-23Crossref PubMed Scopus (73) Google Scholar]. GM crops represent one more tool that farmers have at their disposal to increase productivity and efficiency. For the majority of existing GM crops, a long history of use with alternative technologies to achieve the same benefits exists. For example, GM herbicide-tolerant crops simply expand the herbicide options previously available based on the endogenous tolerance of crops to certain herbicides compared with many weeds. In the area of insect-tolerant crops, pesticides (as well as insect-tolerant crops developed by traditional breeding techniques) have been used for many decades to combat insect pests. There is a long history of developing operational protection goals for these alternative tools (although some alternative tools are not regulated such as pest-resistant and herbicide-tolerant non-GM varieties), and these should serve as a template for evaluating new tools to achieve the same ends. Likewise, the risk–benefit ratio of these existing tools should serve as a benchmark for assessing the safety of new tools that serve the same purpose. If new standards for protection are to be implemented for GM crops, a clear rationale for their development and implementation should be articulated based on rational scientific principles grounded in the context of existing agricultural practices. A balance between risks and benefits should be obtained whenever evaluating the environmental risk of a new technology, and GM crops are no exception. We advocate allowing farmers to address the environmental risks and benefits of agricultural practices for protection goals that are largely restricted to their fields such as maintaining adequate soil fertility and populations of in-field beneficial insects. In these cases, farmers are the main stakeholders and production efficiency should dictate the best management of these practices. For protection goals that extend beyond field margins, and for which multiple stakeholders exist, government regulation may be a good approach. For agricultural practices that directly affect protection goals, straightforward approaches are often available. However, for indirect effects on protection goals, differing approaches are common and are often based on philosophical perceptions rather than objective science. In these cases, we advocate clear identification of protection goals followed by hypothesis-driven experimentation to inform the preferred approach (or approaches) to most efficiently meeting these protection goals while maximizing agricultural productivity. Finally, existing agricultural practices should serve as a model for formulating operational protection goals and assessing the risks and benefits of GM crops. Following a disciplined scientific approach to ERA for GM crops should help resolve controversy in identifying and addressing risk. Through rigorous application of the tried and true scientific method, the risks and benefits of specific GM crops can be objectively evaluated and equitable regulation can be implemented. R.H., R.L., and A.R. are employed by companies that develop and market transgenic seed. M.G.-A. is an independent consultant and has clients that develop and market transgenic seed." @default.
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• W1970542021 title "Bringing policy relevance and scientific discipline to environmental risk assessment for genetically modified crops" @default.
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