Science in Society Archive

The Health and Environmental Impacts of Bt

Lim Li Ching, Institute of Science in Society

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.

Article first published 02/07/02


References

  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,
  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?', I-SIS report, 12 November 2001
  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://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. Tabashnikm 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,
  27. Cummins J (2001) 'Biopesticide and bioweapons', ISIS Report, 23 October 2001,
  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',
  32. 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
  33. 'Pests attack genetically modified cotton', The Jakarta Post, 29 June 2001, www.thejakartapost.com/yesterdaydetail.asp?fileid=20010629.A06
  34. 'GMO brings hardship to S. Sulawesi, farmers claim', The Jakarta Post, 1 June 2002, http://www.thejakartapost.com/yesterdaydetail.asp?fileid=20020601.L03
  35. '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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