10 ecological risk assessment for transgenic crops

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FORUM: Science & Society Ecological risk assessment for transgenic crops: separating the seed from the chaff Rod A. Herman Dow AgroSciences LLC, 9330 Zionsville Road, Indianapolis, IN 46268 An ecological risk assessment for a transgenic crop is required by regulatory agencies worldwide. In certain regions, this includes evaluation of indirect effects of improved pest and weed control on non-target organisms that may use insect pests and weeds as a food source. Here, I consider the merits of providing insects and weed seed as food for a diversity of wildlife within crop fields. Transgenic crops predominate where permitted by gov- ernment regulation. Their rapid adoption in agricultural production is unprecedented [1]. The first wave of input traits provided pest control within crop plants or rendered crops tolerant to more efficacious and ecologically friendly herbicides [2]. However, onerous regulation uniquely applied to transgenic plants, especially in the area of eco- logical risk assessment, has almost prevented the use of this technology in some regions (e.g. The European Union) [3]. Such assessments can include an evaluation of the indirect effects of the improved pestinsect and weed control that are afforded by transgenic cropping systems. Specifically, poten- tial effects on species that feed on the weeds and pests that are reduced in transgenic fields are considered in the eco- logical risk assessment [4]. Here, I briefly discuss the mod- ern agro-ecosystem, and the balance between maintaining high productivity within crop fields and attempting to foster species diversity within agricultural monocultures. Much of our current civilization is associated with a move from a hunter gatherer existence to an agrarian way of life that began approximately 10,000 years ago. The ability to concentrate food production into a limited area reduced the amount of time that was required to gather food from diverse unmanaged habitats. The time saved in gathering food was then available for other activities that allowed the development of civilizations and the concen- tration of population centers [5]. This allowed humans to separate the plants that they needed for food and fiber from the ‘‘chaff’’ (i.e. unwanted material) of the other plants that did not meet their needs. However, maintaining crops is not as simple as planting the seeds of desirable plants in concentrated areas. These crops must be protected from unwanted plants that germinate within the field (weeds) and compete with desirable plants for nutrients, and must also be protected from herbivores and pathogens that compete with people for the plant resources (e.g. insects and diseases). Many techniques mechanical, cultural, biological, and chemical continue to be used to maintain crop pro- ductivity. Transgenic plants are the most recent addition to this tool kit. Transgenic crops most closely resemble the selection of resistant varieties that has taken place over the domestication and improvement of current crop plants [1,6]. From the earliest times, humans saved seed from the most robust and pest-resistant plants [5]. In more modern times, plant breeders have sought out mutant crop plants and wild relatives of crop plants that display pest-resist- ance traits for use in breeding programs. Even more recently, such techniques have been used to select endogenous herbicide-tolerance traits [7]. In these cases, many uncharacterized genes have been moved into com- mercial varieties by traditional breeding to enhance pro- duction. The most recent advancement in crop improvement is the ability to move desirable genes from unrelated species into crop plants, while leaving behind associated genes with unknown or undesirable function. These transgenic crops have been planted widely in those regions that are permitted by government regulations. An ecological risk assessment is required by regulators, and attempts to assess the risk of cultivating a specific transgenic crop on the environment. Two types of effects can occur in the environment: direct and indirect. Trans- genic crops can cause direct effects on a species (e.g. toxicity) or indirect effects caused by elimination of a resource on which a species depends. An example of a direct effect is the dramatic reduction of a corn insect pest, European corn borer larvae, Ostrinia nubilalis, within fields of transgenic maize that expresses Cry1 proteins derived from the microbe Bacillus thuringiensis. Control of certain insect pests is the purpose of these transgenic crops. An indirect effect would also occur on any species that relies on these pests for food (e.g. birds and arthropod predators and parasites) [2]. This is analogous to dramatic- ally reducing mosquito populations in residential areas through spraying insecticides and reduction of larval habitat (e.g. disposing of old tires that hold water). Pre- dictably, species that depend on mosquitoes as a food source (e.g. birds and bats) will be affected. A similar scenario occurs when weeds are controlled within a field by chemical, biological or mechanical means. Species that rely on these weeds for food are affected negatively, and this impact is proportional to the effectiveness of the weed control practice. It should be noted that the abundance of species that depend on crop pests are themselves an arti- fact of the habitat disturbance and concentration of a single plant species intrinsically caused by agriculture. If crops were not planted, insects and weeds on which some organ- isms feed would typically have less suitable habitats. An evaluation of ecological risk depends on some phi- losophical underpinnings. Specifically, one needs to deter- mine our expectations of an agricultural ecosystem. This is Update Corresponding author: Herman, R.A. ([email protected]). TIBTEC-791; No of Pages 2 1

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TIBTEC-791; No of Pages 2

FORUM: Science & Society

Ecological risk assessment for transgenic crops:separating the seed from the chaff

Rod A. Herman

Dow AgroSciences LLC, 9330 Zionsville Road, Indianapolis, IN 46268

Update

An ecological risk assessment for a transgenic crop isrequired by regulatory agencies worldwide. In certainregions, this includes evaluation of indirect effects ofimproved pest and weed control on non-target organismsthat may use insect pests and weeds as a food source. Here,I consider the merits of providing insects and weed seed asfood for a diversity of wildlife within crop fields.

Transgenic crops predominate where permitted by gov-ernment regulation. Their rapid adoption in agriculturalproduction is unprecedented [1]. The first wave of inputtraits provided pest control within crop plants or renderedcrops tolerant to more efficacious and ecologically friendlyherbicides [2]. However, onerous regulation uniquelyapplied to transgenic plants, especially in the area of eco-logical risk assessment, has almost prevented the use of thistechnology in some regions (e.g. The European Union) [3].Such assessments can include an evaluation of the indirecteffects of the improvedpest–insect andweed control that areaffordedby transgenic croppingsystems.Specifically,poten-tial effects on species that feed on the weeds and pests thatare reduced in transgenic fields are considered in the eco-logical risk assessment [4]. Here, I briefly discuss the mod-ern agro-ecosystem, and the balance between maintaininghigh productivitywithin crop fields and attempting to fosterspecies diversity within agricultural monocultures.

Much of our current civilization is associated with amove from a hunter gatherer existence to an agrarian wayof life that began approximately 10,000 years ago. Theability to concentrate food production into a limited areareduced the amount of time that was required to gatherfood from diverse unmanaged habitats. The time saved ingathering food was then available for other activities thatallowed the development of civilizations and the concen-tration of population centers [5]. This allowed humans toseparate the plants that they needed for food and fiber fromthe ‘‘chaff’’ (i.e. unwantedmaterial) of the other plants thatdid not meet their needs. However, maintaining crops isnot as simple as planting the seeds of desirable plants inconcentrated areas. These crops must be protected fromunwanted plants that germinate within the field (weeds)and compete with desirable plants for nutrients, and mustalso be protected from herbivores and pathogens thatcompete with people for the plant resources (e.g. insectsand diseases).

Many techniques – mechanical, cultural, biological, andchemical – continue to be used to maintain crop pro-ductivity. Transgenic plants are the most recent additionto this tool kit. Transgenic crops most closely resemble the

Corresponding author: Herman, R.A. ([email protected]).

selection of resistant varieties that has taken place overthe domestication and improvement of current crop plants[1,6]. From the earliest times, humans saved seed from themost robust and pest-resistant plants [5]. In more moderntimes, plant breeders have sought out mutant crop plantsand wild relatives of crop plants that display pest-resist-ance traits for use in breeding programs. Even morerecently, such techniques have been used to selectendogenous herbicide-tolerance traits [7]. In these cases,many uncharacterized genes have been moved into com-mercial varieties by traditional breeding to enhance pro-duction. The most recent advancement in cropimprovement is the ability to move desirable genes fromunrelated species into crop plants, while leaving behindassociated genes with unknown or undesirable function.These transgenic crops have been planted widely in thoseregions that are permitted by government regulations.

An ecological risk assessment is required by regulators,and attempts to assess the risk of cultivating a specifictransgenic crop on the environment. Two types of effectscan occur in the environment: direct and indirect. Trans-genic crops can cause direct effects on a species (e.g.toxicity) or indirect effects caused by elimination of aresource on which a species depends. An example of adirect effect is the dramatic reduction of a corn insect pest,European corn borer larvae, Ostrinia nubilalis, withinfields of transgenic maize that expresses Cry1 proteinsderived from the microbe Bacillus thuringiensis. Control ofcertain insect pests is the purpose of these transgeniccrops. An indirect effect would also occur on any speciesthat relies on these pests for food (e.g. birds and arthropodpredators and parasites) [2]. This is analogous to dramatic-ally reducing mosquito populations in residential areasthrough spraying insecticides and reduction of larvalhabitat (e.g. disposing of old tires that hold water). Pre-dictably, species that depend on mosquitoes as a foodsource (e.g. birds and bats) will be affected. A similarscenario occurs when weeds are controlled within a fieldby chemical, biological or mechanical means. Species thatrely on these weeds for food are affected negatively, andthis impact is proportional to the effectiveness of the weedcontrol practice. It should be noted that the abundance ofspecies that depend on crop pests are themselves an arti-fact of the habitat disturbance and concentration of a singleplant species intrinsically caused by agriculture. If cropswere not planted, insects and weeds on which some organ-isms feed would typically have less suitable habitats.

An evaluation of ecological risk depends on some phi-losophical underpinnings. Specifically, one needs to deter-mine our expectations of an agricultural ecosystem. This is

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Update Trends in Biotechnology Vol.xxx No.x

TIBTEC-791; No of Pages 2

especially true when considering indirect effects. Is itbeneficial to try to encourage species diversity within acrop field at the expense of productivity? Is it reasonable toprovide habitat that encourages species diversity within amonoculture designed to produce a single product forhuman use? Collectively, is it better to encourage highproductivity on limited acreage at the expense of speciesdiversity within the field, or conversely, to sacrifice pro-ductivity for in-field species diversity, while spreadingcrops across more land?

A basic factor that allowed the development of humancivilizations was the ability to concentrate the productionof food and fiber on limited land. As mentioned above, thisseparated the seed from the chaff that consisted of unde-sirable plants. Further separation of the seed from thechaff occurred as pest and weed control methods wererefined. Plant breeding also resulted in higher harvestindices (i.e. more of the harvestable parts per hectareand per plant), which reduced the chaff even further. Abasic question now exists: do we really want to advocateadding chaff back into our crop fields in the name of speciesdiversity within these fields, or is it better to separate thoselands used for crop production from those used to enhancewildlife diversity? If our goal is to provide weed seed andinsects for wildlife, is it better to do this within crop fields,or is this best done on separate plots of land designed forwildlife and encouraged by programs such as the Conser-vation Reserve Program [8] administered by the UnitedStates government? Taxpayer-funded conservation pro-grams allow resources to be channeled to farmers whoare willing to convert cropland into prescribed habitatspecifically suited for those wildlife species that are valuedgreatest by society. However, it is noteworthy that suchprograms are in contrast with those that seek to beautifythe agricultural landscape or increase agricultural tourismwithout explicit goals related to ecological benefit [9].

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So, how much chaff do we really want in our seed? Itseems like answering the related questions posed herebased on scientific principles, would help to separate theseed from the chaff in the ecological risk assessment oftransgenic crops.

AcknowledgementsI thank Mark Krieger, Barry Schafer, Peter Scherer, Bruce Chassy,Thomas Lyall, Kathryn Clayton, Nicholas Storer, Klaus Ammann, MarkMiles, Wayne Parrott, Brad Shurdut, Jake Secor, and John Cuffe forcomments on a draft of this commentary.

Conflict of interestR. A. Herman is employed by Dow AgroSciences LLC, a wholly ownedsubsidiary of The Dow Chemical Company, which develops transgeniccrops and produces insecticides, herbicides, and fungicides for agriculturalapplications and residential pest control.

References1 Morin, X.K. (2008) Genetically modified food crops: progress, pawns, and

possibilities. Anal. Bioanal. Chem. 392, 333–3402 Ammann, K. (2005) Effects of biotechnology on biodiversity: herbicide-

tolerant and insect-resistant GM crops. Trends Biotechnol. 23, 388–3943 Johnson, K.L. et al. (2006) How does scientific risk assessment of GM

crops fit within the wider risk analysis? Trends Plant Sci. 12, 1–54 Raybould, A. (2007) Ecological versus ecotoxicological methods for

assessing the environmental risks of transgenic crops. Plant Sci. 173,589–602

5 Diamond, J. (2002) Evolution, consequences and future of plant andanimal domestication. Nature 418, 700–707

6 Bradford, K.J. et al. (2005) Regulating transgenic crops sensibly: lessonsfrom plant breeding, biotechnology and genomics. Nat. Biotechnol. 23,439–444

7 Newhouse, K. et al. (1991) Mutations in corn (Zea mays L.) conferringresistance to imidazolinone herbicides. Theory Appl. Genet. 83, 65–70

8 Ribaudo, M.O. et al. (2001) Environmental indices and the politics of theConservation Reserve Program. Ecol. Indicators 1, 11–20

9 Baylis, K. et al. (2008) Agri-environmental policies in the EU andUnitedStates: a comparison. Ecol. Econ. 65, 753–764

0167-7799/$ – see front matter � 2010 Elsevier Ltd. All rights reserved.doi:10.1016/j.tibtech.2010.01.005 Available online xxxxxx