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Bt cotton - bitter harvest
By Mihir Shah & Debashis Banerji, The Hindu, India (24 August 2002)
(http://www.hinduonnet.com/thehindu/2002/08/24/stories/2002082400081000.htm)
FIRST REPORTS from Khargone district of Madhya Pradesh, one of the cotton headquarters of India, endowed with fertile black cotton soil, speak of a 100 per cent failure of the Bt cotton crop. Farmers are up in arms demanding compens7ation from the company that supplied these seeds. While other cotton varieties have also been adversely affected by the drought, they report a failure rate of only around 20 per cent. This is a performance that has shocked even the worst critics of genetically-modified (GM) crops. We do not expect such a complete disaster to be repeated everywhere. But the Bt cotton story in India had all the makings of a terrible tragedy, even before official permission was granted for its cultivation in March 2002.
The tragedy began unfolding in Gujarat where over ten thousand acres of Bt cotton were planted illegally last year. The Genetic Engineering Approval Committee (GEAC) of the Union Ministry of Environment and Forests, whose permission is required for cultivation of any GM crop, ordered the destruction of this illegal Bt cotton. But the decision was never implemented.
In March this year, three hybrid Bt cotton seeds supplied by the Mumbai-based company, Mahyco, were approved by the GEAC for cultivation in central and south India. The U.S. multinational Monsanto has a 27 per cent stake in Mahyco. Bt cotton seeds have been genetically engineered to produce a toxin that can kill the bollworm, a major headache for cotton farmers. They are ineffective against other pests and even according to their suppliers do not have any mechanism to raise yields. The idea is that they would raise the net incomes of farmers since they are expected to reduce spending on pesticides.
But a simple calculation shows that the economics does not quite work out. Seeds currently being used by farmers cost an average of Rs. 325 per hectare.
The pesticide cost is around Rs. 400 per hectare. The Bt cotton seeds are about four times as expe nsive as existing seeds, i.e., Rs. 1,300 per hectare. Some pesticide has to be used even with Bt seeds, particularly because 20 per cent of Bt cotton fields need to be covered with non-Bt seeds (to ensure that pest resistance to Bt cotton does not rapidly develop). Even if Bt seeds are presumed to lead to a dramatic reduction in pesticide costs to say Rs.150 per hectare, the total cost of seeds and pesticides would still be double in the Bt case - Rs. 1,450 compared to Rs. 725 per hectare for seeds currently in use.
The mandatory requirement of growing non-Bt cotton in each Bt cotton plot is based on "resistance management plans" devised in the U.S., where farmers have huge land holdings. The idea is that the surviving resistant insects to the Bt crop will intermate with susceptible ones on the non-Bt crop. But Indian cotton farmers with much smaller land holdings have found it quite impossible to set aside land for these "refugia". Their inability to do so will only accelerate the development of pest resistance to Bt cotton. There are also a large number of technical specifications for refugia management with which Indian farmers have not even been made remotely familiar. This is obviously not a technology meant for the poor, dryland small farmers of India.
Inquiries in the field reveal that the attraction for Bt cotton had much to do with the kind of hype that surrounded its sale. Farmers worried about the cost were falsely promised dramatic increases in yield. Coercion was also employed - availability of credit and other inputs was linked to purchase of Bt. But, most farmers remained unconvinced because of the high price. And this is where the tragedy got really compounded.
Much to the consternation of Mahyco-Monsanto, illegal Bt seeds from last year's Gujarat harvest (that the Government failed to destroy) began flooding the market. A large number of illegal dealers started offering Bt cotton much cheaper, at anywhere between Rs. 100 and Rs. 800 per hectare. In Gujarat last year these seeds were covertly sold under the brand name "Navbharat 151" by the Navbharat Seeds Company. This year, with Bt cotton having being cleared by the Government, and with no action against Navbharat, the seeds obtained from last year's harvest, were openly sold as "Maxi 151" by a Vadodara-based company describing itself as "B.T. Cotton Trial Farm". Its proprietor, Piyush Patel, published huge ads in prominent Gujarati dailies not only extolling the higher yields of "his" Bt cotton, but also claiming its superiority over that supplied by "big companies" (which he described as a "terminator seed").
Following several representations to the GEAC, Mr. Patel was finally arrested in May 2002. But much damage had already been done. Many illegal F2 and even F3 (second and third generation) seeds are reported to have been sold to cotton farmers of Punjab and Haryana, where Bt cotton has yet to be approved. They have also found their way into Maharashtra and Andhra Pradesh. A khadi institute in Gujarat that apparently used last year's Bt seeds, reported uncommon itching and rashes among users of cloth produced from this cotton.
As this illegal trade of bogus operators spread, the Government largely remained a silent spectator. The irony is that those who set so much store by Bt cotton are also passively watching their magic product being made a complete mockery of! We are more concerned that farmers are being taken for a ride. We have consistently argued that any new technology must be introduced only after farmers and consumers have complete information on all its aspects. So that they can make an informed choice. Such a choice has been denied to our people, who are being forced to learn the hard way.
Why can't a large number of public debates be organised in our cotton growing areas, with the participation of the Government, companies, scientists, farmers and consumers? Where this has been done, as in Chitradurga in Karnataka and Medak in Andhra Pradesh, farmers have overwhelmingly rejected GM cr ops.
But the Government has still not placed in the public domain, data generated by Bt cotton trials in India. Ridiculously, the monitoring and regulation of Bt cotton has been entrusted to the very same company that is producing and selling it. Meanwhile, evidence against Bt cotton continues to accumulate worldwide. A study by the Nanjing Institute of Environmental Sciences under the Chinese State Environmental Protection Agency reveals that Bt cotton is harming natural parasitic enemies of the bollworm and seems to be encouraging other pests. The Chinese experience needs to be taken seriously since Bt cotton accounts for more than 1.5 million hectares (35 per cent of total cotton acreage) in that country. The study finds the diversity index of the insect community in Bt fields much lower than in conventional cotton farms in China. It also finds that the populations of pests other than bollworm have increased in Bt cotton fields and some have even replaced it as the primary pest. It would be pertinent to remember that since Bt cotton was developed in the U.S. to tackle only one main pest, the bollworm, its applicability to regions of the world with higher pest diversity was always suspect from the word go. (The writers are scientists in the field of alternatives to genetically-modified agriculture.)
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Part 2
India: Farmers want compensation after ruined GM crops
New Delhi, 6 Sep (IPS/Ranjit Devraj) -- Farmers in India's cotton-growing central and western regions, who were anxious to get genetically engineered cotton seed not so long ago, are now even more anxious about getting compensation from the government for a disastrous failure of this year's crops.
Although the genetically engineered 'Bt cotton' seed was supplied by US seed giant Monsanto through its Indian subsidiary Maharashtra Hybrid Seed Co (MAHYCO), farmers and activists are demanding compensation from the government because it granted the approvals for the seed earlier this year.
Bt cotton seeds are spliced with toxic genes taken from the soil bacterium bacillus thuringiensis, which is capable of killing off the American bollworm pest. However, its resistance to other pests and suitability to Indian climatic factors have never been adequately tested, environmentalists say.
"The seeds of Bt cotton supplied by MAHYCO-Monsanto company failed to give suitable results. The crops in 30,000 hectares all over Vidarbha (farming region in western Maharashtra state) has been spoiled completely by root-rot," said Kishore Tewari, president of the influential Vidarbha Jan Andolan Samiti (People's Movement in Vidarbha).
Tiwari attributed the failure to "wrong selection of Bt genes developed in America and brought to India". He estimated the financial loss to farmers in the Vidarbha region at over $100 million and expected the government to make good.
"We have served a legal notice on the Ministry of Agriculture and if the government does not take cognizance of it, we plan to file a public interest litigation in the Mumbai High Court," Tiwari said.
Monsanto spokeswoman Ranjana Smetacek told IPS that wilting and root-rot were not specific to any particular variety of cotton and has equally affected genetically engineered Bt cotton and ordinary varieties sown side-by-side. Smetacek attributed root-rot to water logging caused by sudden heavy rainfall following a prolonged dry spell, and said that her company planned to release shortly an advertisement advising farmers to drain off excess water from their fields.
Monsanto's explanation was supported by a scientist from the government's Central Institute for Cotton Research (CICR) located in Nagpur, a major city in central India.
"The wilting is not pathogenic and occurs normally when cotton hybrids in the field are exposed to prolonged dry spell followed by heavy showers," said C D Mayee, a scientist at the CICR following surveys in the affected Yavatmal district.
Mayee told IPS that Bt cotton varieties '162' and '184', grown at experimental farms at Saoner and Katol villages 65 km west of Nagpur, were showing no signs of root-rot. But he admitted that the '162' varieties were sensitive to water stagnation. Apart from these two varieties, Monsanto has introduced a third into India.
According to Mayee, it was too early to talk about cotton crop failures in Maharashtra state since the main harvesting season begins in November. He described reports of extensive crop damage in local newspapers this month as "unscientific".
Last month, similar reports of cotton crop failures came from adjoining central Madhya Pradesh state. But Mayee said that he could not comment on crop failures there because his institute had carried out no studies in that state and had no data to go by.
Reports of cotton crop failure in Madhya Pradesh were coming in well before the arrival of this year's delayed monsoons and were attributed to droughts rather than to water logging, and they spoke of the particular vulnerability of Bt cotton varieties.
Mihir Shah, director of the Baba Amte Centre for People's Empowerment and Debashish Banerji of the Samaj Pragati Sahyog (Nature and Society Cooperative), commented in an article in the 'Hindu' newspaper on 24 August that the cotton crop failures in Madhya Pradesh have "shocked even the worst critics of genetically modified crops".
Shah and Banerji, who are themselves based in Madhya Pradesh and scientifically qualified, said that the Bt cotton story in India "had all the makings of a terrible tragedy" that began unfolding in Gujarat state last year. There, 10,000 acres were sown illegally with Bt cotton, with farmers not caring to wait for government approval.
In fact, the Genetic Engineering Approval Committee (GEAC) under the federal Ministry of Environment and Forests ordered the destruction of the illegally grown crops in Gujarat. But that decision was never implemented and in March this year, GEAC cleared Bt cotton for commercial farming against the advice of leading environmentalists.
"The GEAC is solely responsible for hastily pushing in the untested technology despite being warned time and again of the scandal in the name of science," said Devinder Sharma, internationally known campaigner against GM crops and director of the Forum for Biotechnology and Food Security (FBFS), a collective of scientists, farmers, economists and policy makers. Sharma is among those who are demanding that the chairman of the GEAC be held accountable for the present disaster. "This should act as [a] deterrent against the illegal experimentation that goes on unchecked in this country in the name of improving [the] farmers' lot. After all, how many more farmers need to be sacrificed at the altar of agricultural development?"
Sharma pointed out that Indian government agencies had always cited the introduction of Bt cotton in neighbouring China as a reason why it should also be introduced in this country. But, he added, they were silent about recent reports from that country indicating that the crop was environmentally harmful.
The Nanjing Institute of Environmental Sciences reported earlier this year that Bt cotton, which makes up 35% of China's cotton crop, harms the natural parasitic enemies of the bollworm and seems to encourage other pests. According to the report, the diversity index of the insect community in Bt cotton fields was lower than in conventional cotton fields, while the pest dominant concentration index is higher. Bt cotton did not resist bollworm after being planted eight to 10 years continuously, suggesting the build-up of resistance.
Official secrecy has shrouded the entry of Monsanto into India, a recurring theme with Sharma and other environmentalists. Shortly before he resigned as union health minister in June, C P Thakur complained that the Health Ministry was never consulted on the introduction of GM crops. "Genetically modified products could have long-term environmental and health effects. It is essential that the Health Ministry is involved more in such decisions," said Thakur, a successful doctor and researcher in his own right.
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Part 3
The Health and Environmental Impacts of Bt
Lim Li Ching, Institute of Science in Society, PO Box 32097, London NW1 0XR, UK
Transgenic insecticidal crops are genetically engineered to produce an array of insecticidal proteins derived from genes of the bacterium Bacillus thuringiensis (Bt). Bt toxins are stored as inactive crystals (Cry) in bacterial spores, which are activated in the insect gut to create pores on the gut cells, causing an inrush of water that bursts the cell.
The claimed benefits of Bt crops are that the 'in-built' insecticide removes the need to spray broad-spectrum insecticides on the crop, thus reducing insecticide use and providing an efficient means of pest control. There has been widespread planting of three Bt crops - corn, cotton and potato - although other varieties are being field-tested. According to the International Service for the Acquisition of Agri-biotech Applications (ISAAA), of the total 52.6 million hectares of GM crops grown globally in 2001, 7.8 million hectares (15%) were planted to Bt crops, with Bt corn occupying 5.9 million hectares, equivalent to 11% of global transgenic area and planted in six countries [1].
However, there are drawbacks associated with Bt crops. There is evidence of negative impacts of Bt crops on non-target species (including beneficial species), the development of resistance in target pest populations and the toxicity and allergenicity of Bt toxins themselves. The claimed benefits of Bt crops have also been called into question.
Impacts on non-target species
Controversy arose with the publication of a paper in Nature by John Losey and colleagues at Cornell University, in which laboratory studies suggested that Bt corn pollen harmed monarch butterfly larvae [2]. However, in the furore surrounding the debate, the notion of complexity and subtlety in non-target effects was conflated to impacts on monarch butterfly larvae. This narrow view has informed regulatory approval of Bt crops, leading the US Environmental Protection Agency to re-register five Bt corn products for an additional 7 years in October 2001 [3].
The risk assessment that informed this decision claimed, "the impact of Bt corn pollen from current commercial hybrids on monarch butterfly populations is negligible" [4]. It has however been critiqued for focusing on acute toxic effects, while ignoring long-term cumulative and non-linear effects, as well as failing to address impacts on other non-target species and multiplier ecological consequences of all the impacts interacting with each other [5]. Likewise, another study, while acknowledging Cry1Ab as toxic to monarch larvae, but deeming exposure, and hence risk, negligible, concluded that pollen from Cry1Ab, Cry1F and experimental Cry9C hybrids would have no acute effects on monarch butterfly larvae in field settings [6]. It did not consider whether subtle effects could occur when larvae are exposed to low levels of Bt pollen for longer periods (although this is being researched).
Sub-lethal effects cannot be ignored either. A field study investigating the impact of exposure to Bt corn pollen containing Novartis event 176 on two Lepidopteran species, black swallowtails and monarch butterflies, while finding that mortality was independent of proximity to Bt corn and in part due to predation, however also found that Bt corn pollen may have sub-lethal effects on black swallowtails feeding on host plants outside of cornfields [7]. The study found reduction in larval growth rates to be a function of proximity to Bt corn. The likely cause was toxicity because of ingestion of transgenic pollen grains. This conclusion was judged conservative, as repeated rainfalls had occurred during the study, washing away pollen. Furthermore, bioassay indicated that concentrations of event 176 pollen as low as 100 grains/cm2 caused significant mortality in black swallowtails.
Obrycki et al. reviewed the impacts of Bt corn on non-target species, using an ecological approach, rather than a linear toxicological approach focused on corn consumers [8]. Among the evidence reviewed were observations of increased mortality of lacewing (Chrysoperla carnea) larvae when fed on an artificial diet containing Bt toxin or preyed on corn borers or other lepidopteran larvae that had fed on transgenic corn [9]. Potential trophic-level effects of Bt corn on vertebrate predators also need to be considered, because bats and birds are known to prey on larvae and adults of several lepidopteran corn pests. In this respect, the review noted that Bt sprays used to reduce caterpillars in forests led to fewer black-throated blue warbler nests, which in turn would affect breeding activity [10]. Abundance of the parasite Macrocentris cingulum, specific to corn borer larvae, was less in Bt-cornfields compared with non-Bt cornfields, due to significant reductions in larval hosts [11]. Impacts on pollinators, such as bees, and decomposers, need to be better examined and assessed than is done at present.
Bt corn is now the most common management tactic for European corn borer, Ostrinia nubilalis. Impacts on its natural predators and parasitoids cannot be ignored, as widespread planting of Bt corn could create an "ecological desert" with relatively few hosts for natural enemies of corn borer. The negative impact on natural enemies raises the possibility that overuse of Bt corn could lead to resurgence and secondary-pest outbreaks [8].
Research conducted in China by four domestic academic institutions and summarized by the Nanjing Institute of Environmental Sciences, part of the State Environmental Protection Administration of China, showed that whilst Bt cotton is effective in controlling the primary pest of cotton, bollworm (Helicoverpa armigera), and that there are no significant impacts on predatory natural enemies, there are adverse impacts on parasitic natural enemies of bollworm [12]. Furthermore, populations of secondary pests, such as cotton aphids, cotton spider mites, thrips, lygus bugs, cotton whitefly, cotton leaf hopper and beet armyworm, increased in Bt cotton fields after the target pest (bollworm) had been controlled, some of which then replaced bollworm as primary pests and damaged cotton growth. The possibility of outbreaks of certain pests in Bt cotton was deemed much higher, due to lower stabilities of insect community, pest sub-community and pest-natural enemies sub-community, as well as increased pest dominance, in Bt cotton fields than in conventional cotton fields.
Research has also shown that the Cry1Ab protein is released in root exudates from transgenic Bt corn; this is deemed a common phenomenon [13]. The toxin accumulates in soil, as it adsorbs and binds rapidly to soil particles and retains insecticidal activity for at least 180 days. Hence its effects on soil decomposers and other beneficial arthropods may be extensive. Furthermore, Cry1Ab protein exhibits stronger binding and higher persistence, as well as remains nearer the soil surface, in soil with high clay concentrations, indicating that it could be transported to surface waters via runoff and erosion [14]. In contrast, the protein is more readily leached through soil with lower clay concentrations, indicating that it could contaminate groundwater.
Development of resistance
The efficacy of Bt crops will be short-lived if pests evolve resistance to the Cry proteins produced from Bt. Due to commercial growing of Bt crops, the risk of evolution of resistance by pests, increases.
Single-pair crosses with diamondback moth have shown that one autosomal recessive gene can confer extremely high resistance to four Bt toxins (Cry1Aa, Cry1Ab, Cry1Ac and Cry1F) [15]. The research found that a surprisingly high proportion (21%) of individuals from a susceptible strain were heterozygous for the multiple-toxin resistance gene, suggesting that pests may evolve resistance to some groups of toxins much faster than previously expected.
There have also been indications of marked cross-resistance to Cry1Ac developing in Cry1Ab-selected populations of diamondback moths (40-fold, much greater than resistance to Cry1Ab itself) [16]. The mode of inheritance of resistance to Cry1Ac in diamondback moths was traced to inheritance as an incompletely dominant trait. The extent of dominance of resistance to Cry1Ac depended on the toxin concentration - resistance was recessive at high doses, but almost completely dominant at low doses. Results suggested that more than one allele on separate loci were responsible for the resistance.
Research from China has verified that cotton bollworm can develop resistance to Bt cotton and scientists concluded that Bt cotton would probably lose its resistance to bollworm in fields after 9 years of continuous planting on a large scale [12]. While Bt cotton demonstrated excellent resistance to the second generation of bollworm, the resistance of Bt cotton to bollworm decreased over time, and control is not complete in the third and fourth generations, necessitating chemical use then. Furthermore, it was suggested that bollworms developed resistance more quickly on transgenic Bt cotton than with topical Bt sprays, possibly because Bt spray contains several insecticidal crystal proteins and insect exposure to the toxin is over a short time. In contrast, transgenic Bt cotton contains one insecticidal crystal protein (Cry1Ac) and the toxin is expressed throughout the entire growing season.
Management strategies based on refugia and high-dose, where regular influx of susceptible insects dilutes the frequency of resistance alleles, assume that inheritance of resistance is recessive. If non-recessive inheritance of resistance is common in field populations of insects (as demonstrated by [16]), then current resistance management strategies may be ineffective. More so given anecdotal evidence that farmers in India may not even follow guidelines of 20% refuge stipulated by regulatory authorities for the planting of Bt cotton [17] and that it would be difficult for farmers in China to implement a refuge system under prevailing small-plot cultivation conditions [12].
Another strategy being developed is to 'stack' or 'pyramid' genes encoding different Cry proteins. This means using multiple resistance genes in a given line. However, given that cross-resistance is known to occur for some Bt proteins, reliance upon this approach is deemed "somewhat short-sighted" [18] by the same scientists who claim in a review that commercial large-scale cultivation of current Bt corn does not pose a significant risk to the monarch population, or to other non-target insects.
Toxicity of Bt
While Bt is rarely associated with disease in humans, in actual fact Bt-toxins are actual and potential allergens for human beings. Field workers exposed to Bt spray experienced allergic skin sensitization and induction of IgE and IgG antibodies to the spray [19]. This demonstrates that Bt is able to penetrate the human body and elicit an immune response.
In light of these findings, a team of scientists have cautioned against releasing Cry-containing plants and plant products for human use. These same scientists have also demonstrated that recombinant Cry1Ac protoxin from Bacillus thuringiensis is a potent systemic and mucosal immunogen, as potent as cholera toxin. Administration of recombinant Cry1Ac to mice intraperitoneally or intragastrically induced systemic and intestinal antibody responses [20]. Cry1Ac enhances mostly serum and intestinal IgG antibody responses, especially at the large intestine, and its effects depend on the route and antigen used [21]. Further research showed that that intranasal, rectal and intraperitoneal application of Cry1Ac to mice resulted in the production of antibody responses (IgM, IgG and IgA) at several mucosal sites (in the serum, vaginal and tracheobronchial washes and in the fluids of the large and the small intestine) [22].
A Bt strain that caused severe human necrosis (tissue death) killed mice infected through the nose within 8 hours, from clinical toxic-shock syndrome [23]. The combination of infection with Bt and influenza A virus (IAV) killed 40-100% of mice, depending on the concentration of Bt spores and strains used [24]. Although Bt 3a3b (from biopesticide) seemed to be less virulent than Bt H34 (isolated from human infection), even a low inoculum of the bacterium was able to seriously complicate IAV respiratory tract infection in mice. This has implications for human exposure to Bt, especially for immunocompromised people.
Both Bt protein and Bt-potato harmed mice in feeding experiments, damaging their ileum (part of the small intestine) [25]. Both the groups of mice fed Bt potatoes or potatoes spiked with Bt toxin revealed common features such as the abnormal appearance of mitochondria, with signs of degeneration and disrupted short microvilli (microscopic projections on the cell surface) at the surface lining the gut [26].
Because Bt and Bacillus anthracis (the anthrax species used in biological weapons) are closely related to each other and to a third bacterium, Bacillus cereus, a common soil bacterium and cause of food poisoning, they exchange plasmids (circular DNA molecules containing genetic origins of replication that allow replication independent of the chromosome) bearing toxin genes readily [27]. In the event that B. anthracis mated to transfer plasmids to B. thuringiensis, recombination could create plasmids bearing toxins both for anthrax and for killing insects. New strains of B. anthracis with unpredictable properties could arise.
Questionable benefits
Evidence suggests that the use of Bt corn will not significantly reduce insecticide use, despite claims otherwise [8, 28]. Similarly, data on transgenic cotton show that although to date one fourth of American cotton is produced with Bt varieties, no significant reductions in the overall use of insecticides were achieved [29].
A survey using crop data from 2000 found no economic advantage for Iowa farmers to plant Bt corn [30]. While average yield for Bt corn was higher (152 bushels per acre vs. 149 bushels for non-Bt), seed and fertilizer costs for Bt corn averaged $4.31 and $4.63 per acre more, respectively, than for non-Bt corn. A farm-level economic analysis of Bt corn also demonstrated less net profit, lower corn prices and lost corn exports [31]. According to this analysis, from 1996-2001, American farmers paid at least $659 million in price premiums to plant Bt corn, while boosting their harvest by only 276 million bushels - worth $567 million in economic gain.
Thus, the economic benefits of using Bt corn are not assured. Only during years when corn borer densities are high does Bt corn crops out-yield the non-transgenic. Obrycki et al. assert that given the limited benefits for insect management and the documented ecological effects of transgenic insecticidal corn on non-target species, Bt will only have a limited role in management of lepidopteran pests in corn [8].
There are reported failures of Bt crop performance (where Bt cotton has been attacked by pests) [32] and poor yields trapping farmers in debt [33] in Sulawesi, Indonesia. Other unexpected impacts are pseudopregnancies and reduced farrowing rates in swine, which have been related to high levels of Fusarium mycotoxins and possibly traced to Bt corn hybrids [34]. This is a puzzling phenomenon, as Bt corn is supposed to have less Fusarium contamination and lower levels of mycotoxins than conventional corn (because Bt corn is not supposed to experience corn borer injury that leads to elevated Fusarium infection). Many questions remain unanswered on this issue.
1. 'Global GM crop area continues to grow and exceeds 50 million hectares for first time in 2001' ISAAA press release, 10 January 2002, http://www.isaaa.org/press%20release/Global%20Area_Jan2002.htm
2. Losey JE, Rayor LS and Carter ME (1999) 'Transgenic pollen harms monarch larvae', Nature 399: 214.
3. 'Biotechnology corn approved for continued use', EPA press release, 16 October 2001, http://yosemite1.epa.gov/opa/admpress.nsf/b1ab9f485b098972852562e7004dc686/8db7a83e66e0f7d085256ae7005d6ec2
4. Sears MK, Hellmich RL, Stanley-Horn DE, Oberhauser KS, Pleasants JM, Mattila HR, Siegfried BD and Dively GP (2001) 'Impact of Bt corn pollen on monarch butterfly populations: a risk assessment', PNAS 98(21): 11937-42.
5. Ho MW and Cummins J (2001) 'Bt risk negligible?', ISIS report, 12 November 2001, www.i-sis.org.uk
6. Hellmich RL, Siegfried BD, Sears MK, Stanley-Horn DE, Daniels MJ, Mattila HR, Spencer T, Bidne KG and Lewis LC (2001), 'Monarch larvae sensitivity to Bacillus thuringiensis purified proteins and pollen', PNAS 98(21): 11925-11930.
7. Zangerl, A.R., McKenna, D., Wraight, C.L., Carroll, M., Ficarello, P., Warner, R. and Berenbaum M.R. (2001) 'Effects of exposure to event 176 Bacillus thuringiensis corn pollen on monarch and black swallowtail caterpillars under field conditions', PNAS 98(21): 11908-12.
8. Obrycki JJ, Losey JE, Taylor OR and Jesse LCH (2001) 'Transgenic insecticidal corn: beyond insecticidal toxicity to ecological complexity', BioScience 51(5): 353-361.
9. Cited in Obrycki et al. (2001): Hilbeck A, Baumgartner M, Fried PM and Bigler F (1998a) 'Effects of transgenic Bacillus thuringiensis corn-fed prey on mortality and development time of immature Chrysoperla carnea (Neuroptera: Chrysopidae)', Environmental Entomology 27: 480-487; Hilbeck A, Moar WJ, Pusztai-Carey M, Filippini A and Bigler F (1998b) 'Toxicity of Bacillus thuringiensis Cry1Ab toxin to the predator Chrysoperla carnea (Neuroptera: Chrysopidae)', Environmental Entomology 27: 1255-1263; Hilbeck A, Moar WJ, Pusztai-Carey M, Filippini A and Bigler F (1999) 'Prey-mediated effects of Cry1Ab toxin and protoxin and Cry2A protoxin on the predator Chrysoperla carnea', Entomologia Experimentalis et Applicata 91: 305-316.
10. Cited in Obrycki et al. (2001): Rodenhouse NL and Holmes RT (1992) 'Results of experimental and natural food reductions for breeding black-throated blue warblers', Ecology 73: 357-372.
11. Cited in Obrycki et al. (2001): Pilcher CD (1999) Phenological, physiological, and ecological influences of transgenic Bt corn on European corn borer management, PhD dissertation, Iowa State University, Ames, IA.
12. Xue D (2002) 'A summary of research on the environmental impacts of Bt cotton in China', Nanjing Institute of Environmental Sciences, http://a1584.g.akamai.net/7/1584/1533/7d224b99a880be/www.greenpeace.org/~geneng/reports/env_impact_eng.pdf
13. Saxena D, Flores S and Stotzky G (2002) 'Bt toxin is released in root exudates from 12 transgenic corn hybrids representing three transformation events', Soil Biology and Biochemistry 34(1): 133-137.
14. Saxena D, Flores S and Stotzky G (2002) 'Vertical movement in soil of insecticidal Cry1Ab protein from Bacillus thuringiensis', Soil Biology and Biochemistry 34(1): 111-120.
15. Tabashnik BE, Liu YB, Finson N, Masson L and Heckel DG (1997) 'One gene in diamondback moth confers resistance to four Bacillus thuringiensis toxins', PNAS 94: 1640-1644.
16. Ali H Sayyed and Wright DJ (2001) 'Cross-resistance and inheritance of resistance to Bacillus thuringiensis toxin Cry1Ac in diamondback moth (Plutella xylostella L) from lowland Malaysia', Pest Management Science 57: 413-421.
17. Sahai S (2002) 'The economics of Bt cotton', AgBioIndia Mailing List, 19 June 2002, www.agbioindia.org
18. Gatehouse AMR, Ferry N and Raemaekers RJM (2002) 'The case of the monarch butterfly: a verdict is returned', TRENDS in Genetics 18(5): 249-251.
19. Bernstein I, Bernstein J, Miller M, Tiewzieva S, Bernstein D, Lummus Z, Selgrade M, Doerfler D and Seligy V (1999) 'Immune responses in farm workers after exposure to Bacillus thuringiensis pesticides'. Environ Health Perspect 107: 575-82.
20. Vázquez-Padrón RI, Moreno-Fierros L, Neri-Bazán L, de la Riva G and López-Revilla R (1999) 'Intragastric and intraperitoneal administration of Cry1Ac protoxin from Bacillus thuringiensis induce systemic and mucosal antibody responses in mice', Life Sciences 64(21): 1897-1912.
21. Vázquez-Padrón RI, Moreno-Fierros L, Neri-Bazán L, de la Riva G, López RE and Villa R (1999) 'Bacillus thuringiensis Cry1Ac protoxin is a potent systemic and mucosal adjuvant', Scandinavian Journal of Immunology 46: 578-584.
22. Moreno-Fierrosa L, Garcíaa N, Gutiérreza R, López-Revillab R and Vázquez-Padrónc RI (2000), 'Intranasal, rectal and intraperitoneal immunization with protoxin Cry1Ac from Bacillus thuringiensis induces compartmentalized serum, intestinal, vaginal and pulmonary immune responses in Balb/c mice', Microbes and Infection 2: 885-890.
23. Hernandez E, Ramisse F, Cruel T, le Vagueresse R and Cavallo JD (1999) 'Bacillus thuringiensis serotype H34 isolated from human and insecticidal strains serotypes 3a3b and H14 can lead to death of immunocompetent mice after pulmonary infection', FEMS Immunology and Medical Microbiology 24: 43-7.
24. Hernandez E, Ramisse F, Gros P and Cavallo JD (2000) 'Super-infection by Bacillus thuringiensis H34 or 3a3b can lead to death in mice infected with the influenza A virus', FEMS Immunology and Medical Microbiology 29: 177-181.
25. Fares NH and El-Sayed AK (1998) 'Fine structural changes in the ileum of mice fed on dendotoxin-treated potatoes and transgenic potatoes', Natural Toxins 6: 219-33.
26. 'Bt is toxic', ISIS News 7/8, February 2001, www.i-sis.org.uk
27. Cummins J (2001) 'Biopesticide and bioweapons', ISIS Report, 23 October 2001, www.i-sis.org.uk
28. Benbrook, C.M. (2001) 'Do GM crops mean less pesticide use?' Pesticide Outlook, October 2001.
29. Thalmann, P. & V. Kung (2000) 'No reduction of pesticides use with genetically engineered cotton', WWF International, www.biotech-info.net/WWF_inter_update.pdf; and Thalmann, P. & V. Kung (2000) 'Transgenic cotton: Are there benefits for conservation? A case study of GMOs in agriculture, with special emphasis on freshwater', www.panda.org/resources/publications/water/cotton/transgenic.html
30. Duffy, M. (2001) 'Who benefits from biotechnology?' Presented at the American Seed Trade Association meeting, 5-7 December 2001, Chicago, http://www.leopold.iastate.edu/pubinfo/papersspeeches/biotech.html
31. Benbrook, C.M. (2001) 'When does it pay to plant Bt corn: farm-level economic impacts of Bt corn, 1996-2001',
www.gefoodalert.org/library/admin/uploadedfiles/When_Does_It_Pay_To_Plant_Bt_Corn.pdf or www.biotech-info.net/Bt_corn_FF_final.pdf
32. 'Pests attack genetically modified cotton', The Jakarta Post, 29 June 2001, www.thejakartapost.com/yesterdaydetail.asp?fileid=20010629.A06
33. 'GMO brings hardship to S. Sulawesi, farmers claim', The Jakarta Post, 1 June 2002, http://www.thejakartapost.com/yesterdaydetail.asp?fileid=20020601.L03
34. 'Pseudopregnancies puzzle swine producer', Iowa Farm Bureau Spokesman, by Tom Block, 29 April 2002, http://www.ifbf.org/publication/archive/t_search1.asp?number=19120&atype=current
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