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The Rationale for Ecological Monitoring

The monitoring of crops is not new. In 1845, when the potato blight that would eventually decimate Irish agriculture first appeared in fields on the Isle of Wight, its arrival was promptly noted in the Gardener's Chronicle of London. “Mycologists raced to see who could first identify the fungus that was on the potato leaves,” Paul Waggoner, of the Connecticut Agricultural Experiment Station, told the workshop audience, “and within a year one had published a drawing and a Latin inscription in the very first volume of the new Journal of the Horticultural Society.” In the 20th century, Waggoner said, monitors have spotted such pests and pestilences as Dutch elm disease, the gypsy moth, the corn borer, the boll weevil, Medfly, the Japanese beetle, and the Southern corn leaf blight. Those are examples of a type of ad hoc monitoring. Its purpose is to watch for specific things that can go wrong so that people can respond appropriately. Often such monitoring is no more sophisticated than when farmers observe their crops and report anything unusual.

A second type of monitoring is more systematic and directed. Referred to as "accountant" or "scientific" monitoring by various speakers, its purpose is to gather data to build a detailed understanding of what is going on in a field or in the surrounding area. “Accountants require consistent and comparable records,” Waggoner said; that is why, for example, the US Department of Agriculture (USDA) has collected data on farming for more than a century. “Reports of crop yields and area began in the time of Lincoln,” Waggoner said; “reports of fertilizer and pesticide use began in the time of Kennedy. Without these data series, one cannot separate anec-



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Page 4 The Rationale for Ecological Monitoring The monitoring of crops is not new. In 1845, when the potato blight that would eventually decimate Irish agriculture first appeared in fields on the Isle of Wight, its arrival was promptly noted in the Gardener's Chronicle of London. “Mycologists raced to see who could first identify the fungus that was on the potato leaves,” Paul Waggoner, of the Connecticut Agricultural Experiment Station, told the workshop audience, “and within a year one had published a drawing and a Latin inscription in the very first volume of the new Journal of the Horticultural Society.” In the 20th century, Waggoner said, monitors have spotted such pests and pestilences as Dutch elm disease, the gypsy moth, the corn borer, the boll weevil, Medfly, the Japanese beetle, and the Southern corn leaf blight. Those are examples of a type of ad hoc monitoring. Its purpose is to watch for specific things that can go wrong so that people can respond appropriately. Often such monitoring is no more sophisticated than when farmers observe their crops and report anything unusual. A second type of monitoring is more systematic and directed. Referred to as "accountant" or "scientific" monitoring by various speakers, its purpose is to gather data to build a detailed understanding of what is going on in a field or in the surrounding area. “Accountants require consistent and comparable records,” Waggoner said; that is why, for example, the US Department of Agriculture (USDA) has collected data on farming for more than a century. “Reports of crop yields and area began in the time of Lincoln,” Waggoner said; “reports of fertilizer and pesticide use began in the time of Kennedy. Without these data series, one cannot separate anec-

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Page 5 dote and rumor from genuine trends." The second, scientific sort of monitoring was the major focus of the workshop. “We are talking about more than just waiting for things to appear; we are talking about a proactive monitoring regimen,” said Barbara Schaal, of Washington University. Is this sort of monitoring of genetically engineered crops necessary? After all, it is more difficult to carry out, requires a more sustained effort, and demands a higher level of scientific sophistication than simply acting as a sentinel. If it is necessary, why? What should it be looking for? The workshop participants were asked first to address these basic issues. They found the third question perhaps the easiest to answer because there is already widespread agreement in the field as to what sorts of effects might be expected to accompany the cultivation of transgenic crops. For Bt corn and other crops that have been genetically modified to produce a pesticide, one of the biggest concerns is that widespread use of the crop could lead to the evolution of pests that are resistant to the pesticide. That is of particular concern for organic farmers, said Mark Lipson, of the Organic Farming Research Foundation, because they use the Bacillus thuringiensis (Bt) bacterium as a natural pesticide. For reasons that are not understood, the bacteria produce a variety of substances that are toxic to caterpillars and many other insects, so dusting with Bt allows organic farmers to protect their fields without using chemical pesticides. A second concern is that crop plants that have been genetically modified to resist herbicides could turn into hard-to-control weeds in succeeding years when their fields are devoted to other crops. “Some of these volunteers can be quite serious,” said Peter Day, of Rutgers University, using the term—volunteer—that agricultural scientists use to refer to crop plants that establish themselves without human intervention. “Volunteer potatoes are sometimes a nuisance in succeeding cereal crops, for example, and might have to be dealt with by herbicide treatment.” Both risks are expected to affect mainly farmers. Being resistant to a pesticide is not likely to make a difference in an insect's survival away from a farm, where pesticides are not used. Similarly, crop plants that have been genetically engineered to be resistant to herbicides would be no more likely than nonresistant plants to invade the areas surrounding the farm. But transgenic crops might affect ecosystems away from the farm in various ways, and these must be watched for as well. One example is the possibility that Bt toxin in the drifting pollen of transgenic corn is killing monarch caterpillars. That is a case of what researchers refer to as "effects on nontarget organisms." Of course, chemical pesticides might also kill nontarget organisms and can drift from farmers' fields, but the development of plants that produce toxic pollen is a new phenomenon in agriculture. Another concern about transgenic plants centers on horizontal gene-

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Page 6 transfer, that is, the movement of genes from the genetically modified plants to organisms in the surrounding environment. That can happen, for instance, when a virus infects a plant that has been given a viral gene to protect it from a particular virus. Through the process of recombination, the invading virus can add that viral gene to its own complement of DNA and turn it into a new—and possibly more threatening virus. “When the first reports of recombination between a virus and a viral transgene came out, it was thought to be quite anomalous,” said Alison Power, of Cornell University. “Now if you talk to molecular virologists, most of them will argue that, sure, it is going to happen. Recombination is going to occur between these viral transgenes and wild-type invading viruses.” Horizontal gene transfer can also occur between crop plants and closely related weeds. “Essentially every crop that we have in our array of domesticates is associated somewhere on the planet with a companion weed,” said Hugh Wilson, of Texas A&M University. Those companion weeds are so closely related to the crop that they can hybridize and share genes. Queen Anne's lace is a companion weed to the carrot, for instance, and Johnson grass is a companion weed to sorghum. Generally, the companion weed is descended from the same undomesticated plant that served as the starting point for breeding the domesticated crop, and often the crop and the companion weed have passed genes back and forth over time, so neither can be considered the progenitor of the other. If a transgenic crop is planted in an area with its companion weed, chances are that the transgene will eventually be passed on to the companion weed. Thus, if the domestic squash is genetically engineered to be resistant to a particular type of virus, sooner or later its companion weed, the Texas gourd, will pick up that same viral resistance. And the viral resistance offers a large enough competitive advantage, Wilson noted, that one line of Texas gourd could displace others, and this would lead to a loss of genetic diversity in the gourd. That is worrisome, he said, because when a problem appears in the domesticated crop—a major blight, for instance— plant breeders must be able to fall back on the broader gene pool of the undomesticated relatives for help in breeding plants that are resistant to the problem. “If we don't have that variation as a bank to go get things that we may need in the future, then we have a problem.” Genes also flow freely among different varieties of the same crop plant, so a farmer growing nontransgenic corn, for example, might find that because his neighbor had planted transgenic stock, his own fields contained some transgenic plants. Or two transgenic varieties could swap transgenes. “There are five herbicide-tolerant canolas on the market in Canada," said Rob MacDonald, of Aventis, and sometimes different varieties are grown in neighboring fields. “One of the risks is the potential development of multiresistant populations of canola due to gene flow

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Page 7 between nearby or adjacent fields." A line of canola plants that was resistant to several major herbicides could be a particularly troublesome weed in fields that were planted with another crop. The planting of strategic areas in which nontransgenic crops act as “buffer” zones may be critical to the management of gene flow or pollen migration. Thus, the potential consequences of planting transgenic crops are in four major categories: the development of pesticide resistance in crop pests, the transformation of crops into invasive weeds, harm to nontarget organisms, and gene flow from crops into related plants, viruses, or other organisms. If monitoring is to be done, those are the major things to look for. Without monitoring, it may be hard to know just how much of a threat each of those possible consequences poses. To some degree, the threat can be assessed by field tests before a genetically engineered variety is released for commercial use, and that is regularly done. But, Schaal noted, such testing cannot catch everything. “On an overall time scale, the prerelease testing is relatively short. It also involves small numbers of plants. But once the organisms are released into the environment, we are dealing with large numbers of individuals, and we are dealing with a long time span, so different scientific aspects come into play. Things that have low probabilities become much more likely when you have large numbers. Also, small effects that can accumulate over time will become apparent over a long period. So we are dealing with a different set of issues when we do ecological monitoring. We don't know whether such effects occur, but we need to have the kind of monitoring that will detect if such small effects begin to accumulate or such improbable events begin to appear.” Besides such issues of scale, the complexity of ecosystems is another argument for monitoring, Schaal said, because laboratory or field tests will never fully replicate all the interactions among organisms in an ecosystem. “The only way to see what happens in an ecosystem is to place the genetically modified crop into an ecosystem. We cannot predict what the outcome will be, so we need to have some sort of monitoring to be assured that we can detect any kind of untoward effects.” In particular, a technique called risk assessment is used to estimate the likelihood that a transgenic problem might damage the environment in some way, and risk assessment, said Bob Frederick, of the Environmental Protection Agency (EPA), demands the sort of data that only detailed monitoring can provide. “Monitoring is a critical component of risk assessment.” Calculating the risk of any particular event demands knowledge of two factors, Frederick noted: the probability of the event, and the hazard that event poses. If, for example, one wished to estimate the risk posed by cultivating a variety of squash that had been genetically engineered for resistance to a particular virus, one would begin by deter-

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Page 8 BOX 1: Traditional Agriculture and the Environment With all the attention paid to possible effects of transgenic crops, it is easy to forget that traditional agriculture's effects on the environment have been nothing short of overwhelming. And, given the proven ecological consequences of traditional agriculture, some researchers at the workshop wondered why transgenic crops should be subject to so much more scrutiny than traditional crops. “Tens of thousands of years ago, humans were hunter-gatherers,” noted Peter Day, of Rutgers University, “and as they learned to save seeds and plant stocks for their first attempts at cultivation, they laid the foundation for plant domestication, plant improvement, and what we today call plant breeding. The ecological impacts of agriculture that resulted from this transition were profound. As the human population grew, it altered the face of the earth.” As Europeans colonized the New World, some 20,000 cultivated plants were introduced into North America and South America, noted Anne Vidaver, of the University of Nebraska, Lincoln. This has reshaped the ecology of the Americas, Vidaver said, from the plants themselves to the insects that depend on them for food, and down to the microorganisms that live on and in the plants. The effects continue today. On farms, the cultivation of traditional crops can have many of the same ecological consequences that have triggered concern about transgenic crops. As Norm Ellstrand, of the University of California, River side, pointed out, traditional farming practices have at times led to the creation of troublesome weeds. “There was an introduction of a forage grass called Michel's grass to the northwestern United States in the 1930s,” he said. “This hybridized with cultivated rye, and it gave rise to a new weed that altered the economics of the region such that farmers were unable to grow either rye or wheat in that region.” There have been cases where cultivated crops were introduced into a region and wiped out a wild relative, thus diminishing genetic diversity. “The spread of rice cultivation in Taiwan led to the extinction of a wild subspecies of Oryza sativa,” Ellstrand noted. Furthermore, the use of chemical herbicides can cause weeds to mining the probability of resistance transfer from modified squash to companion weed. Next, one would determine the hazard that such acquired resistance would present. Might it cause a loss of genetic diver sity in the companion weed? If so, would that matter, and how much? Could the weed become a greater pest in agricultural fields, and how difficult would it be to deal with? Answering any of those questions, from the probability of an event to the degree of hazard that it represents, requires data on the plants and other organisms and how they interact with one another. And those data, Frederick said, can be obtained only through monitoring. Furthermore, in practice, the risk posed by a particular crop can depend critically on how the crop is managed, said Fred Gould, of North

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Page 9 evolve resistance to them, and the chemical pesticides can kill desirable insects in much the same way that Bt corn pollen is thought to dispatch monarch caterpillars. Given that traditional agriculture is not without its own risks, one audience member asked whether there is anything inherent in the development of transgenic crops that warrants monitoring them more closely than traditional crops are monitored. “Many of us take the view that the answer to your question is no, there isn't anything special,” Day replied. “Transgenic crops are different. Can one say that they are 100% safe? No. One cannot say that of traditional crops, either. So it comes down to one's assessment of the appropriate risk. One needs data to satisfy people's concerns.” In the workshop's wrapup session, MacDonald, of Aventis, echoed that sentiment. “One of my conclusions from the workshop,” he said, “is a clear consensus that our agricultural systems do have substantial impact on ecological systems regardless of the technologies that are used—conventional, no tillage, conservation tillage, genetically modified, or organic for that matter." Thus, he said, monitoring decisions should be based on the product itself and not on the process by which it was derived. Another view expressed by panel member and farmer David Winkles, of the South Carolina Farm Bureau, was that the benefits of genetically modified crops outweigh any theoretical ecological hazards and that monitoring is generally unnecessary. Thomas Nickson, of Monsanto, summed up his point of view by asking a question: “Is it appropriate or even possible to defocus on our fixation with genetically modified crops and step back into the larger system of food production, so that we are dealing with the more important problems? I'm talking specifically to the science community rather than the public at large, because I think the public has a legitimate and genuine concern over genetically modified foods for numerous reasons. But for scientists, is it appropriate—and is it possible—-to have this defocusing?” Carolina State University. In the case of a crop genetically engineered to produce its own pesticide, such as the Bt toxin, it is possible to prevent insects from evolving resistance to that pesticide by maintaining refugia— in this case areas planted with crops that do not produce the pesticide—so some percentage of the insects in the fields do not feel any selective pres sure to develop such resistance. But if this sort of risk management is to be successful, Gould said, it is necessary to monitor the insects for signs of emerging resistance and to maintain the refugia accordingly. "Monitor ing is a very important component here.” In addition to those scientific rationales, there are good social reasons for monitoring. The ecological monitoring of genetically modified crops is more than a scientific issue, noted William Hallman, of Rutgers Univer-

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Page 10 sity. Policies about transgenic crops are influenced by a number of factors, including public attitudes toward the crops, and, Hallman said, public attitudes depend on factors other than scientific ones. “From a social-psychological perspective, why monitor?” he asked. “One of the answers is that the public wants us to. Even if there is nothing there, monitoring sends the signal that we take this seriously enough to make sure that nothing bad will happen—that we don't expect something bad to happen, but we want to make sure. We take this seriously.” Thus, according to Hallman, even if genetically modified crops pose no greater threat to the environment than conventional crops, there remains a reason to treat the transgenic crops differently. The public sees them as something different—and potentially more dangerous—and rigorous monitoring can help to reassure members of the public that scientists are being careful to safeguard them.