Thank you for this opportunity to present the view of Consumers Union on the vital need to preserve the efficacy of Bacillus thuringiensis. We commend the EPA for convening the SAP to address the lack of proven and effective resistance management plans for the planting of Bt-transgenic plant varieties.
The EPA has raised a number of intriguing technical questions regarding the possible efficacy of Bt resistance management plans (RMPs) based on the high dose plus refugia strategy. While these questions warrant further research focus, they obscure what is really important about this two-day meeting.
EPA's conditional registration of Bt-transgenic cotton and corn was based on the requirement that proven, effective RMPs be in place. The burden was squarely placed on the manufacturers, and for good reason. The emergence of resistance to a valuable fruit, vegetable and field crop biopesticide like Bt poses significant and long-term risks. This is because resistance to Bt will inevitably lead to greater reliance on conventional insecticides, many of which pose significant risks to consumers and the environment-risks the EPA is struggling to contain through implementation of the Food Quality Protection Act. Resistance to Bt will remove a valuable and safe tool, thereby increasing the pressure borne by other insecticides and control strategies. The lessons of the last 40 years have confirmed over and over that the greater the pressure on a given set of pest management tools, the sooner some will start falling by the wayside.
Once resistance genes emerge and gain a foothold in populations, they cannot be recalled. Hence, risks following Bt resistance are open-ended and essentially permanent. Risks to a conventional pesticide, on the other hand, are typically limited to certain circumstances of use and location, and can be truncated quickly by stopping further use of a product.
For this reason, EPA must act with great prudence in protecting the efficacy of Bt. The past year's scientific discoveries cry out for a decisive response by EPA. The Agency needs to hear your views on a fundamental question-even with better knowledge and refinements in today's RMPs, do you really think they will work?
In the Preamble of your report to EPA, we urge you to speak clearly to this key question-In your judgement, can a practical RMP be devised and implemented that will, with a high degree of certainty, assure that Bt will remain effective for 20, 30, or 50 years? (By "high degree of certainty," we mean something like a 90 percent chance of success or better).
A clear statement of your view on this matter is needed if there is to be any chance of compelling the Agency to take actions that will be very unpopular and strongly opposed in some quarters.
Consumers Union's Position on Bt-Transgenics
Consumers Union published in October 1996 a major report on Integrated Pest Management entitled Pest Management at the Crossroads (PMAC). This report describes in detail the reasons why Bt-transgenic plant varieties are not a sustainable technology, and will furthermore likely trigger resistance. The consequences are of deep concern to Consumers Union, and will result in increased reliance on high-risk organophosphate and carbamate insecticides. It is for this reason that PMAC offers the following recommendation on page 247:
"Revoke Certain Transgenic Plant Approvals. EPA should suspend or revoke registrations for previously approved Bt-transgenic plants, and those for herbicide tolerant crops when there is credible evidence that the transgenic plant variety is likely to worsen resistance to any currently registered active ingredient."
At the time PMAC was completed, we felt decades of experience with resistance mechanisms and limited evidence on Bt-resistance pointed clearly to potential problems with Bt-transgenics. At the most basic level, the notion of Bt-transgenic crops makes little or no ecological sense, and Bt-transgenics are inherently incompatible with the basic principles of IPM.
The primary basis of any RMP for pesticides is to use the pesticide as sparingly as possible, with use reserved only when necessary to avoid economic loss and then only in parts of the field where absolutely needed, i.e. pesticide use should be minimized in both space and time so as to minimize selection pressure for the evolution of resistance. In addition, when a biopesticide like Bt is applied as a standard foliar spray, it diversifies the pest management tools drawn upon by farmers and reduces the burden placed on any one tool. Spreading out the pest management burden in this way makes good ecological-and practical-sense. It increases the chance of success across a wide range of circumstances over time.
Bt-transgenic crops produce Bt endotoxin continuously throughout their tissue during the entire crop season, i.e. the pesticide (Bt endotoxin) is not minimized in space or time. It is produced and present whether needed or not. In spite of this basic ecological problem, the companies all developed RMPs that are similar. Each is based on theoretical models that contains a number of key assumptions, some of which have recently been shown to be more leaps of faith than reasonable, science-based judgements.
EPA registered the crops, particularly cotton and corn, with the condition that the companies develop and have in place scientifically grounded, proven RMPs. Yet, we are starting into the third commercial year of Bt-transgenic crops and recent field data have irrevocably undermined several key assumptions supporting high dose/refugia.
Granted, EPA has raised several relevant and interesting questions about existing RMPs-but the answers probably will not change the outcome if this experiment is allowed to go on. We think that the best and most up-to-date science points clearly to the conclusion that widespread planting of Bt-transgenics will lead to resistance. It matters little if a RMP delays resistance for two, three or five years. At best, manufacturers hope their RMPs might sustain Bt efficacy for up to 10 years. The loss of Bt will thereafter be essentially permanent, and will trigger all sorts of difficulties in the decades ahead in managing a wide range of lepidopteran insects.
The four key assumptions that underlie the RMPs for all transgenic crops released so far are:
Industry urges farmers not to worry because new technologies and biopesticides will be available as older ones lose effectiveness. They are, in effect, asking consumers and farmers to give up a sure-bet for a roll of the biotech dice. Public health officials said the same thing about human antibiotics 15 years ago and now we are down to one for some ailments.
Assumptions No Longer Supported By Field Data
Assumption 1. The "high doses" achieved in transgenic plants in greenhouse and controlled field trials would also constitute "high doses" in commercial fields.
Data from the present Bt-transgenic crops show that this is not always the case. For both cotton and corn, Bt endotoxin expression starts out high in most fields but tapers off as the season progresses. In cotton, expression tends to be much lower-and sometimes below a lethal dose-in the bottom 25 percent of the plant. Furthermore, what constitutes a "high dose" in the lab may not constitute a "high dose" in the field due to lower susceptibility of wild populations of lepidopteran larvae to the endotoxin. This particularly appears to be true for the cotton bollworm, Helicopvera zea.
Plus, any source of stress, injury or pest damage that damages part of a plant will lead to differential toxin levels and some non-lethal foliage, which insects seem able to find (what Marvin Harris calls "behavioral resistance").
Assumption 2. An unsprayed refuge covering 5 percent to 15 percent of a
planted field will be adequate to assure the rare resistant survivor will
mate with a susceptible insect.
As we heard in discussion yesterday and today, and given the scientific studies contained in the UCS publication Now or Never, both the size and structure of refuges is highly problematic. Indeed the studies presented in Now or Never propose that refuges need to be much larger than EPA presently requires, especially for cotton.
Assumption 3. Natural resistance to Bt is a rare recessive trait that carries significant genetic load.
Surprisingly, few data exist on frequency of Bt resistance alleles in wild lepidopteran population. Two studies published last year demonstrated that resistance to Bt is not as rare as previously suspected. Dr. Gould and colleagues reported that the frequency of the major Bt resistance gene in a field population of Heliothis virescens was about 0.0015 (Gould et al., 1997). Dr. Tabashnik and colleagues showed that the frequency of a multiple-toxin resistance allele in susceptible populations of the diamondback moth was an astonishing 0.120.
The susceptible populations of diamondback moth that Dr. Tabashnik worked with had been reared for over 100 generations without exposure to Bt. The fact that the resistance allele had such a high frequency strongly suggests that the resistance gene carries very little, if any, genetic load. As Dr. Tabashnik et al. concluded, "Extended maintenance of a resistance allele frequency close to 0.10 without exposure to Bt implies that in the absence of Bt [sic], heterozygotes have little or no fitness disadvantage relative to susceptibles" (Tabashnik et al., 1997a: 1643). If this finding turns out to be true for other lepidopteran species, it has grave implications for the high dose plus refugia RMP strategy.
Another disturbing finding from Dr. Tabashnik et al.'s work was that Bt resistance worked differently in a Philippine population of diamondback moth, compared to Hawaii and Pennsylvania populations. First, cross resistance didn't readily occur. Second, resistance to endotoxins Cry1Aa and Cry1Ac did not behave as recessive traits; indeed resistance to Cry1Aa behaved as a dominant. If resistance is a dominant trait, then the high-dose/refugia strategy will be severely weakened. The results from the Philippines show that not only do other mechanisms of resistance to Bt occur, they also do not necessarily act as recessive traits. Thus, one cannot assume much about the exact nature of Bt resistance in wild populations of lepidopterans; only empirical field data will suffice. The lack of such data for the pests of Bt corn and cotton should be grounds alone to revoke the registrations.
Assumption 4. Resistance to different strains of Bt endotoxin will require separate independent mutations.
Work on diamondback moth has clearly shown this assumption to be false. Dr. Tabashnik et al.'s work (Tabashnik et al., 1997a,b) found that diamondback moth "populations from Hawaii and Pennsylvania share a genetic locus at which a recessive mutation associated with reduced toxin binding confers extremely high resistance to four Bt toxins" (Tabashnik et al, 1997b: 12780). Furthermore, data from a Florida population of diamondback moth demonstrated similar results (Wang et al., 1997). At the recent Entomological Society meetings in Nashville, TN, Dr. Tabashnik stated that he expected that findings similar to his would emerge in ongoing work with several other lepidopteran species.
Additional Evidence
The recent work of Dr. Angelika Hilbeck of the Swiss Federal Research Station for Agroecology and Agriculture has shown that Bt-corn can adversely impact populations of key beneficial insects. In a number of trials, Dr. Hilbeck reported 60 percent to 65 percent mortality among lacewing larvae that fed on lepidopteran larvae reared on Bt corn.
Summary
In summary, for the reasons outlined above, we feel that EPA has no choice other than to revoke the conditional registrations for Bt transgenic crops until such time as the Agency has sufficient evidence that the resistance management plans (RMPs) are scientifically grounded and proven effective.
References
Gould, F., Anderson, A., Summerford, D., Heckel, D., Lopez, J., Micinski, S., Leonard, R. and M. Laster. 1997. Initial frequency of alleles for resistance to Bacillus thuringiensis toxins in field populations of Heliothis virescens. Proceedings of the National Academy of Sciences, 94: 3519-3523.
Tabashnik, B., Liu, Y.B., Finson, N., Masson, L. and D.G. Heckel. 1997a. One gene in diamondback moth confers resistance to four Bacillus thuringiensis toxins. Proceedings of the National Academy of Sciences, 94: 1640-1644.
------------------------------, Malvar, T., Heckel, D.G., Masson, L., Ballester, V., Granero, F., Mensura, J.L. and J. Ferre. 1997b. Global variation in the genetic and biochemical basis of diamondback moth resistance to Bacillus thuringiensis. Proceedings of the National Academy of Sciences, 94: 12780-12785.
Tang, J.D., Gilboa, S., Roush, R.T. and A.M. Shelton. 1997. Inheritance, stability, and fitness of resistance to Bacillus thuringiensis in diamondback moth (Lepidoptera: Plutellidae). Journal of Economic Entomology, 90: 732-741.