September 1998 ROBIN JENKINS Bacillus thuringiensis, a biopesticide used by gardeners for several generations, has recently become the latest shining star for agrochemical and biotech companies. Having been cast aside and almost forgotten when synthetic pesticides were introduced, it has recently experienced a meteoric rise to stardom, especially in the hands of genetic engineers. But stardom does not suit Bt and its fame is not likely to lead to fortune, either for farmers or agbiotech companies. Robin Jenkins examines the history of Bt and the implications of its sudden and widespread application to a myriad of crops around the world. Bt is short for Bacillus thuringiensis, a naturally occurring soil bacterium which is fatal to the grubs of a wide range of insects, including many butterflies, moths, weevils and beetles. It is of particular interest to farmers, foresters and horticulturists because it is effective against many of the pests which commonly attack commercially important crops such as maize, rice, cotton and potatoes. Organic gardeners have used Bt for a couple of generations. The Bt poison is only activated within the gut of particular insect grubs and has no deleterious effect on other species. Its biologically effective life is short and if it is not eaten by a grub within a few days it becomes ineffective. The poison is thus harmless to all but the target grubs and unlike many chemical and biological pesticides, it does not directly harm the carnivorous insects and grubs which would normally control the population of plant-eating grubs. The word "directly" is stressed because there is now circumstantial laboratory evidence that insects that have eaten grubs which have in turn ingested Bt can suffer biological disadvantages as a result. The advantage of using a biopesticide like Bt is that it is fairly specific and quite lethal. Bt particularly suits integrated pest management (IPM) and ICM (Integrated Crop Management) strategies because it is only effective directly against the pest. This encourages farmers to intervene only when there is a pest problem rather than to spray their fields with poisons as a standard precaution. There are also several disadvantages to Bt: wind and rain can sharply reduce its effective biological life; the pest has to attack the crop before Bt can be used, so some damage is always sustained; grubs that eat the underside of the plant foliage can escape a Bt spray or dusting; and insects that bore into the plant can escape the effects altogether. The traditional use of Bt by organic farmers and horticulturists has thus been limited to the control of pests that eat the outer leaves of plants. Pests that burrow into the plant such as the European corn borer or the rice borer can withstand traditional Bt sprays or dustings. 1913-1940: The Age of Innocence Bt was first isolated in 1913, when its capacity to kill certain insects in their grub stage was noted. The bacterium is easily propagated and can be used as a powder or in a water solution. Within a few years of its discovery, Bt became commercially available and was used mainly by vegetable growers to eliminate caterpillar infestations before the advent of chemical pesticides. The producers of Bt were typically small family firms operating by mail order. Bt was simply one product in the wide armoury of naturally-occurring insecticides that were commonly used before DDT ushered in the age of synthetic insecticides during World War II (WWII). For the more sophisticated grower, Bt offered an advantage over nicotine or pyrethrum in that it was fatal only to a small range of insects and left beneficials such as lacewings and ladybirds untouched. Products sold on the market probably consisted of mixtures of strains in unknown proportions, resulting in differences in the efficacy of different Bt products. Bt was thus a somewhat hit or miss product. Some growers swore by it; others regarded it as pretty useless. There is no evidence of large scale use of Bt for the first 50 years of its known existence, nor of any systematic research on the various strains of Bt in existence. No one understood why it worked or how it worked, so no one could explain why it sometimes worked effectively, whilst at other times this was not the case. There was nothing intrinsically ecological or organic about the use of Bt up to WWII. Indeed, had Bt been more reliably effective, it might well have become part of the pesticide treadmill a long time ago. As it happens, Bt did not reach the level of regular, extensive use required to encourage the biological success of resistant insect populations until quite recently. Luckily - as it turns out - Bt was used intermittently and sparingly, so it survived as a useful insecticide. But it is important to note that the survival of Bt up to WWII was a good accident rather than the result of consciously good practice. 1940-1960: Embracing Synthetic Pesticides Bt was eclipsed by synthetic insecticides from WWII through to the publication of Rachel Carsons "Silent Spring" in 1962. For some 20 years, Bt was only of interest to those growers who did not want to use synthetic insecticides. During this period, the arguments of those who refused to use the synthetic products were easily marginalised as "unscientific", "folksy" or just plain "backward." They could give no scientific explanation as to why their methods sometimes worked or sometimes failed to work. Furthermore, there was no pressure to find alternatives to synthetic pesticides since the evidence we now have about their widespread harmful effects simply did not exist. In addition, the new synthetic products were reliable, effective and their mode of action was generally understood. After a generation of largely uncritical use, however, two difficult facts about the synthetic insecticides had to be acknowledged: - they caused widespread biological destruction and environmental pollution way beyond their insect targets - resistant mutations in the target insect population became dominant and rendered the products useless The search for alternatives had started. 1960-1990: Bt Becomes Big Business For reasons that no one seems able to explain, until quite recently it was widely believed by entomologists that Bt was not only an environmentally-friendly biopesticide, but also one to which insects would not adapt. Unlike chemical pesticides, Bt was presumed to remain permanently effective. It was described as "the wonder pesticide" and the panacea for many of the ills of the pesticide industry, even though the majority of insect pests were, and probably always had been, naturally resistant to Bt. A few chemical majors, such as Abbot Laboratories, BASF, Novo Nordisk, and Sandoz, started moving into Bt. Research on Bt strains and targets started and the market for Bt in forestry and vegetable production grew rapidly. Inevitably, the persistent use of Bt season after season soon resulted in resistant insects, the first one being the Diamond-back Moth common in the Far East and Oceania. The Diamond-back Moth already had a reputation for getting around chemical pesticides faster than most other insect pests and early reports of its resistance to Bt sprays were greeted with dismay. Bt had been used most intensively in Hawaii, which soon became a centre for studies of insect resistance to Bt. The response of the agrochemical industry was typically up-beat. It claimed that Bt could easily be bred to produce thousands of genetically different strains and so keep ahead of the resistant insects. It was a strategy particularly suited to the economic interests of the largest players in the Bt market because they had the advantage of the biggest R&D budgets. The small, traditional producers were thus marginalised and different strains of Bt such as Bt israelensis and Bt kurstaki began to appear on the market. It looked as though the biological obsolescence of successive Bt strains might conveniently dovetail with the economic need for the growth and technological development so critical to keep the pesticide industry thriving. The new strategy was effective for marginalising the small producers of Bt but it did not last for long. Evidence soon came in that insects resistant to one strain of Bt could also be resistant to other strains, even those with which they had never been in contact. The biochemistry of the Bt poison turned out to be too complicated for the agrochemical industry. Panic soon set in. A working party on Bt resistance was set up by the industry to commission further research, and more importantly, to keep the agricultural authorities at bay. In most countries, pesticide safety requires the authorities to limit the use of those pesticides to which resistance has evolved. No one in the industry wanted to be presented with a list of crops on which Bt could not be used. The working party was very productive: it resulted in an enormous increase in research on Bt, and the production of literally hundreds of articles in a variety of scientific journals. But at the end of all this endeavour, resistance to Bt remains a problem, and the transfer of resistance from one Bt strain to another remains a mystery. This in turn is used as a justification for more research rather than tighter controls. Meanwhile, the scientific agenda has become almost the same as the agenda of the agrochemical industry: the questions that now occupy the minds of the entomologists are those that most affect the profits of the agrochemical companies. There are no global statistics on the application of microbial Bt. In the USA, 57 crops were being treated with Bt sprays on 2,037,834 acres by 1992. Eight crops artichokes, aubergine, cabbage, cauliflower, celery, collards, spinach and sweet peppers were heavily dependent on Bt, with more than 80% of planted areas being sprayed in one or more states. California is the biggest producer of vegetables in the USA and Bt is used very widely (see Table 1). Much of the impetus to use Bt so widely comes from the food industry, and supermarkets in particular, which demand unblemished produce at any cost. Although no incidence of insect resistance has been reported in California to date, it will only be a matter of time before the problem emerges, and given the figures on usage, the problem will probably start with artichokes, aubergines and collards. Table 1. Use of Bt Sprays in California 1992 Source: Gianessi.L and Anderson.J. (1995) Pesticide Use in US Crop Production, National Center for Food and Agricultural Policy, Washington DC It is clear that the widespread utilisation of Bt sprays in California already risks putting Bt onto the pesticide treadmill for a fairly wide range of insect pests. While California may be leading the way, farmers in many other parts of the world are experiencing the same problems. They start with conventional chemical pesticides and when there are no effective chemicals left, they resort in desperation to Bt. And the problem is now getting much more serious. The use of Bt sprays is fast being eclipsed by Bt plants: Bacillus thuringiensis has now fallen into the hands of the genetic engineers. The heavy focus on Bt by large agrochemical and biotech corporations is illustrated by the huge number of patents taken out on it. Up to June 1998, 482 patents had been submitted or awarded mentioning Bt. Some 95 of these patents involve transgenic plants. The top ten patentees hold 62% of all patents, with Dow alone controlling one fifth of them. Table 2: Bt: one microbe, 482 patents Company Patents Dow AgroSciences 98 Novartis 36 Monsanto 25 Novo-Nordisk 25 AgrEvo (Hoechst-Shering) 24 EcoGen 22 Inst.Appl.Microbiol.Russia* 22 Toa-Synth.Chem. 20 Advanta 15 Inst.Pasteur 12 * Joining several microbiology research centres in Russia Source: Derwent biotechnology abstracts, June 98 1990-2005? The short era of Bt plants All the crops on which Bt is currently used can be turned into Bt plants by genetic engineering. Not content with Bt field crops such as potatoes and maize, the industry is now developing Bt fruit trees such as apples, nut trees such as walnuts and even Bt timber such as poplar and spruce. Table 3. Bt Crops in field tests up to 1997 Alfalfa Allegheny S Berry Apple Aubergine Broccoli Cotton* Cranberry Grape Maize* Peanut Poplar Potato* Rapeseed Rice Spruce Tobacco Tomato Walnut * in production 1996 Source: ISB Environmental Release Database, USDA. (www.aphis.usda.gov/bbep/bp/index.html) The question of how to classify a Bt plant or tree divides the USA and the EU, resulting in the application of entirely incompatible legislation on either side of the Atlantic. According to the US, a Bt plant is an insecticide, subject to US legislation on pesticides. According to the EU, Bt plants are genetically engineered organisms and subject to GMO legislation. Greenpeace has taken the French Minister of Agriculture to court for refusing to treat a Bt maize developed by Novartis (Ciba-Geigy-Sandoz) as an insecticide, while the Washington-based International Center for Technology Assessment has taken the US Environment Protection Agency to court for not enforcing resistance management strategies for Bt crops. The principle of the genetic engineering is quite simple. The Bt gene that codes for the desired poison (there are several molecular variations) is isolated and then added to the genetic information already possessed by the plant. The plant then expresses the Bt poison, making it fatal to the target insect. If the story ended there it would be worth a good chapter in any history of agriculture because it would represent a significant advance in our ability to compete with our insect competitors. In practice, future generations will almost certainly view this latest innovation as mistaken and reckless, if not entirely stupid and unforgivable. Why? A plant which expresses Bt poison throughout its growing life provides the strongest possible biological advantage to Bt-resistant insects over and above the normal vulnerable insects in the population. It is therefore likely to result in Bt resistant insects much, much faster than even the inappropriate and regular use of Bt sprays. A panel of 14 eminent entomologists convened by the US Environmental Protection Agency in February 1998 agreed that the appearance of Bt-resistant insects on major crops such as cotton, potatoes and maize was inevitable. The important questions were how the onset of resistance might be delayed, and what should be done once resistant insects had been identified. They spent two days deliberating these questions and were unable to agree a common set of recommendations. The Union of Concerned Scientists (UCS) published a 149-page report in advance of the hearing, arguing for strict controls in order to help save Bt as a biologically-useful biopesticide. Focusing on cotton, maize and potatoes, the UCS strategy relies on the provision of non-Bt plant refuges in which the Bt-vulnerable insects can continue to multiply, thus reducing the rate at which the Bt-resistant insects dominate the population. It is a last ditch attempt to save Bt, since Bt plants are already being grown on a grand scale in the US. In 1997, farmers sowed about 2.8 million hectares of Bt maize, 680,000 hectares of Bt cotton and 10,000 hectares of Bt potatoes. The eminent entomologists on the EPA panel were under intense pressure to come up with a refuge strategy that the industry finds commercially acceptable. However, there is little evidence other than from controlled experiments in laboratories that any of the refuge strategies proposed will extend the useful life of Bt by more than a few years. Nevertheless, nervous companies selling Bt products are grasping at the life vest thrown out, and Novartis recently offered farmers a financial incentive to adopt refuge strategies. NOVARTIS GRASPS THE LIFE VEST In a desperate attempt to ward off obsolescence in its newly-launched Bt maize, the agrochemical giant Novartis has started to offer farmers financial incentives to adopt refuge strategies for their crops. Growers who buy a significant amount of Bt seed will be offered 'substantial' savings if at least 20% of their order includes non-Bt hybrids. Although Novartis is attempting to paint this move in a positive light, it is the action of a corporation in a state of panic. In the US, Bt maize has been rapidly swept up by farmers. In 1996, it accounted for less than 1% of all US production. In just two years, this figure had risen to 19%. Now that the resistance problem has been widely acknowledged, Novartis is grasping at straws to save its genetic masterpiece. The company is recommending that farmers adopt their insect resistance management (IRM) stewardship programme by planting up to 40% of their total maize crop to non-Bt maize. The need to offer a financial incentive demonstrates that farmers are not voluntarily adopting the refuge strategies recommended by the seed companies, probably because they are too complex for use in a commercial farming situation. Novartis states that 'We didn't make an insect resistance management recommendation until the scientific community developed a research-based recommendation.' This is a stark admission that the technology was introduced before proper research had been done. To anyone following transgenic crop releases, this does not come as a surprise, but it contrasts starkly with the industryís recent media campaign claiming that genetically-engineered products have been subject to rigorous testing. Novartis proudly claims that it was 'the first seed company to publicly support a science-based IRM strategy.' This confirms something else we already know: that science-based strategies are something of a rarity in the biotech industry. Who knows, maybe, just maybe, they might learn something from this. Source: Novartis press release In Europe, the biotechnology industry is having a difficult time bringing Bt plants to market (see box). Novartis Bt maize has been the subject of intense controversy ever since it was first proposed. The only reason it has been approved is because a loop-hole in the EU decision-making machinery allowed it through, despite the opposition of a majority of Member States. However, the 1998 season has been a more or less complete failure for Bt maize in Europe, thanks to the action of Confederation Paysanne activists, who rendered practically the entire Novartis stock unusable and received suspended prison sentences for their pains. In the Far East, the International Rice Research Institute (IRRI) has been producing Bt rice. IRRI openly admits to the resistance problem in a pamphlet: As in the case with all insecticides, insect pests will eventually develop resistance to Bt toxins. It is not possible to predict how long Bt rice will remain effective, but the development of pest resistance to Bt toxins can be slowed by careful design of Bt rice plants and use of appropriate strategies for the deployment of these plants in farmers fields. Anticipating criticism, the IRRI pamphlet concludes that: No evidence exists to suggest that stem borers that evolve resistance to Bt toxins will become more damaging to conventional rice varieties, but the evolution of stem borer resistance to Bt toxins will of course decrease the effectiveness of Bt rice ... Bt rice is not expected to reduce the effectiveness of Bt toxins for control of pests in other crops. 2005-2010: Replacement of Bt by Phl? Hope springs eternal. The UKs Farmers Weekly of July 24, 1998, headlines an article: New insecticide might end fears of Bt gene over-use. But there is nothing particularly new about this latest wonder pesticide that promises to solve the Bt resistance problem. Photorhabdus luminescens (Phl) is a bacterium which produces four toxic proteins. It lives inside nematodes which have been used by organic gardeners for the control of insects for some time. Now Dow AgroSciences and the University of Wisconsin have isolated the active ingredients with a view to replacing the Bt market with Phl. The show goes on . Lessons to be Learned The agrochemical industry takes the pesticide treadmill for granted as an inevitable fact of life. It is a convenient belief for companies which base their profits and growth on the planned or unplanned obsolescence of their products. In fact, the treadmill is a self-fulfilling prophecy. The industry might even manage to keep ahead of the mutant insects that conveniently open up new markets by making old pesticides obsolete. These companies are now in the business of commercialising a range of traditional biopesticides that have been used by peasants and organic gardeners, sometimes for generations. They privatise this traditional knowledge, make global markets out of the products and because of the resistance syndrome, and end up destroying any possibility of using the biopesticides in a traditional, sustainable manner. 'GENETIC HOOLIGANISM' IN THE UK Maybe it's the late summer weather or the poor showing in the World Cup, but all of a sudden the UK has been seized with a fit of gardening, that most English of pastimes. Unlike our US cousins who are positively swamped with mutant corn, soya and rape but are leaving it alone, the English activists' favourite game is "hunt the gene fields." There are currently 300 sites licensed for the deliberate release of genetically engineered (GE) plants in the UK. These comprise around 100 test sites where 13 biotech companies are going through the motions prior to colonising European soil. So far around 36 have been set upon with broomsticks, sickles and weeding gloves. Genetically engineered food, as most UK consumers will tell you, is a US imposition, and 77% want it banned. More than 90% want to be able to choose not to eat it. When the first ships of GE soybeans reached our shores, Greenpeace blockaded them. A week later Earth First!ers and striking dockers occupied the unloading cranes. A few weeks later, protesters daubed red Xs for "genetic Xperiment" on some of the silos. The silos contained "a dangerous contaminant," explained the activists' press release, and safety experts tried to work out what had been added to the soybeans for a week. The answer of course was in the genes. That was 1996. Fast forward two years and many actions later and there are currently around 20 autonomous anti-biotech groups in the UK, aside from the bigger multi-issue campaigning groups. Much of the action focuses on supermarkets which are blockaded every weekend, while spoof "disloyalty" cards are distributed and "contaminated" stickers are put on particularly offensive brands. When these actions began, all the supermarkets said that segregating GE beans from natural beans wassn't possible and anyway they were safe. Now at least one has guaranteed its own brand free of GE ingredients, and others are scrambling to follow suit. The gene activists are clearly winning the battle of ideas, but the biotech barons are still striding ahead in terms of sheer acreage. With the enclosure of the genetic commons, protesters are returning to the fields. One field of GE maize was visited by 600 local people, some of whom closed their shops to make the trip. The field is within pollination distance of the country's largest organic farm, where corn is grown. Under threat of losing his organic status, the affected farmer and local campaigners took the government to court. The GE maize was proven to be illegal as the UK government had broken its own regulations. It has since been destroyed, not by the courts of course, as should have happened, but by 20 people one summer evening. Not surprisingly, the increasing number of nighttime raids has led to calls by agrobiotech companies for greater secrecy and protection. Every crop destroyed can set back research up to five years, and damages are currently estimated at around $25,000 per decontamination. The accusation of "ecoterrorism" has been leveled at activists, and Monsanto has dubbed us "scientific hooligans." Source: Jim Snail (1998). "Hey USA: Get ... Into your Genes," article for Earth First! Journal. Bt is the first biopesticide to have been globally commercialised and it is the very act of such widespread commercialisation that undermines its biological effectiveness. The bigger the Bt market, the quicker the insects become resistant to Bt. The sustainable use of effective biopesticides is simply not compatible with free market economics. It seems quite likely that the agrochemical industry will end up making a loss from their Bt and Phl investments. Then it will be the task of governments and international agencies to deal with the mess, as they are currently doing for the first round of Green Revolution pest control strategies. Perhaps then a more rational system for the use of biopesticides on a sustainable basis will emerge. In the meantime, ordinary people all over the world are being robbed of freely existing, sustainable and ecologically harmless methods of controlling insect pests. As a result, our environment is biologically poorer, our agriculture is more precarious and our insect competitors are more effective. Robin Jenkins is working on a study of the socio-economic implications of Bt, funded by the DG XII (Science Ministry) of the European Commission. He can be contacted at La Ferme Paulianne, Luc-en-Diois, 26310, France. Email: [email protected] Sources: * M Mellon & J Rissler (1998). Now or Never: Serious New Plans to Save a Natural Pest Control. Union of Concerned Scientists, Washington, USA. * IRRI (1997). Bt Rice: research and policy issues. IRRI Information Series No 5, Box 933, Manila 1099, Philippines. * G Persley (1996) Biotechnology and Integrated Pest Management. CAB International, Oxford UK. * B Tabashnik (1994). Evolution of Resistance to Bt. Annual Review of Entomology 39: 47-79. * J Mendelson (1998). Testimony before the US EPA Scientific Advisory Panel on Bt. ICTA, Washington DC. * A Hruska (1997). Transgenic Bt Plants in Mesoamerican Agriculture. Libreria Zamorano, Box 93, Tegucigalpa, Honduras. * Novartis (1997). Le livre vert du Mais Cb. Novartis Seeds, BP27, 31790 Saint Sauveur, France. * US EPA (1998). White Paper on Bt plant pesticide resistance management. US Environment Protection Agency, Washington DC.