To Bt or not to Bt: The Sound Science that brought down Bt Crops

Since the publication of Losey's study in the journal Nature showing that Bt-corn pollen harms monarch butterflies, things have gone into a downward spiral for Bt-crops.  Bt-corn is now banned in Austria, France and Germany, and Monsanto's Bt-potato division has been closed down by its new parent company, Pharmacia.

'Bt' is short for Bacillus thuringiensis, the soil bacterium providing the genes for making toxins that kill insects; different forms of which are incorporated into GM crops. The adverse environmental impacts of Bt crops are now well documented in the scientific literature, ranging from harm to non target organisms to the evolution of resistance in insect pests, making it necessary to plant a high proportion of non-Bt crop for 'resistance management'. Aberrant gene expression in the field results in low-dose varieties which are ineffective in pest control and foster resistance. 

Cross pollination with non GM varieties creates Bt-weeds, and the Bt-plants themselves cause major problems as volunteers.  Active Bt  toxin leaks from plant roots into the soil where it is not biodegradable and  accumulates over time.  This will have major impacts on soil health,  with knock-on effects on all other trophic levels of the ecosystem. The recent report that a GM  gene has transferred from GM pollen to microbes in the gut of bee larvae underlines the fact that Bt toxin genes, like all other GM genes, will  spread out of control.   The case for withdrawing all Bt-crops is now compelling.

The way the case has been built is exemplary of the power of good independent science, which is indispensable for sound policy decisions.

No less than eighteen Bt crops were approved for field testing by the US Dept. of Agriculture between 1987 and 1997 (1).  Bt cotton was the first to be approved for commercial use (USA 1995), followed by corn, potato and tomato.

The first specific concerns on the safety of Bt crops were raised from within the scientific community in 1997 when Angelicka Hilbeck and colleagues (2) showed that lacewings fed on pests that have eaten Bt-maize took longer to develop and were two to three times more likely to die.

Organic farmers also started to voice their fears - they have been using the spores of Bacillus thuringiensis as an occasional insecticide spray.  Their fear was founded in the rapid development of resistance to Bt toxin in pest populations continuously exposed throughout the GM plant's growing season, with the potential loss of their only organic insecticide.  They were also worried about GM contamination via cross-pollination - now admitted as unavoidable by our regulators.

Then came Losey's famous Monarch butterfly study (3), which was confirmed by another from  the University of Iowa (4), showing that milkweed in and at varying  distances from Bt crops in the field does cause an increase in mortality to Monarch butterflies.  Milkweed samples were taken from within and at the edge of the Bt corn field and were used to assess mortality of first instar monarch, D. plexippus exposed to Bt and non-Bt corn pollen.

Within 48 hours, there was 19% mortality in the Bt corn pollen treatment, compared to 0% on non Bt-corn pollen exposed plants and 3% in the no pollen controls.  This second study counters all the spurious arguments that the Losey's study was a 'worse case scenario' that bears no relevance to field conditions.  Besides which, when Losey conducted his experiments he did not spatula Bt pollen on to the leaves of milkweed, as was reported by industry, he dusted the leaves in accordance with levels observed in the field.

In a desperate recent attempt to counter this evidence, the pro-biotech lobby has just released a story claiming that pollen from Bt corn does not harm the black swallowtail. This story has been thoroughly deconstructed (see "Tale of the Swallowtail", this issue).

The biotech industry is fully prepared to misreport research results in order to confuse and mislead the public.  On Nov 2nd 1999, a scientific meeting took place in Rosemount, Illinois, to discuss Bt corn and monarchs.

That same morning, all the major news desks round the US received a fax carrying a News article about the meeting - which had only just begun at that point - headlining 'Researchers conclude Bt corn poses little risk to Monarchs'.

Luckily, Carol Yoon of the NY Times was at the meeting and received word from her editor in New York.  She asked the participants if they agreed with what was obviously a press release from industry.  The answer from the floor was a resounding "No" - her report was the only accurate account of the meeting, but unfortunately, the majority of US citizens got the industries' take on it (5).

After months of heated debate on the effects of Bt on non-target insects, the US Environmental Protection Agency (EPA) convened a Scientific Advisory Panel (SAP) meeting in Dec 1999 and asked the panel to review EPA's non-target organism testing requirement, applicable to Bt crops.  The panel found EPA requirements inadequate and urged the agency to substantially expand the scope and quality of the studies that it relies upon (6).

Plans for managing the development of Bt-resistance in insect pests have been actively debated in the scientific literature, and earlier this year, the EPA revised their original mandate and ruled for larger refuges of non GM crop planted with the GM crop. This was hailed as a step in the right direction and now refuges have to be at least 20%.   But major controversies remain as to whether or not the refuges should be sprayed by conventional insecticides (7).   A study in the University of Arizona (8) showed that boll worm larva fed on GM and non GM develop at different rates and it is highly unlikely that they will interbreed, dashing any hopes of diluting out or slowing down the evolution of resistance.  These moths mate within three days of hatching and the males only live for a week. Also, dilution only works if the Bt-resistance is recessive, ie, requiring two copies of the resistance gene to be expressed, and the EPA's resistance management program relies on the trait being recessive.

Unfortunately, studies on the inheritance of Bt resistance showed that it is a dominant trait (9) as insects with only one copy of the resistance gene survive exposure to Bt.  Low levels of Bt expression in Bt crops has also been documented and also serves to foster resistance.

Other scientists (10) have designed elaborate choice experiments that seek to understand insect behavior in terms of 'pollen avoidance', which will affect the evolution of Bt-resistance. However, by their own admission, these data can not be used to arrive at any conclusions about the effects of Bt toxin-containing pollen. This work does however highlight the need to consider complex behavioural as well as toxicological aspects.

In June1999, Monsanto applied for the first Experimental Use Permit on CRY3Bb transgenic corn,  another Bt corn line aimed at corn rootworm.  The application has been thoroughly assessed by an alliance of four independent non profit organizations (11), who report the most astonishing findings. The technical study submitted by Monsanto in July 1999 contained no molecular data, nor data on the breeding regime, for three different Bt lines.  Data on the levels of protein expression in different tissues was included. But 300 corn plants were produced for only two of the transformation experiments, and some of the critical measurements of expression levels were done on only two plants.  Despite this, the data clearly indicate that different transformations led to significantly different levels and patterns of protein expression.  Such differences are of crucial important in assessing efficacy, resistance management and non-target impacts, as well as changes in the microflora of the digestive systems of livestock and humans using the crop for food.

Monsanto then submitted its application in full in August 1999, moving from greenhouse-scale research to unrestricted field use in one year.  In the covering letter they wrote; "Please note that approval of this registration by May 2000 would reduce the need for additional submissions and reviews for year 2000 field trials".   This statement makes it blatantly obvious that Monsanto has no intention of investigating their findings any further with respect to health and environmental impacts. To date their application in full is still pending in the US  but has been granted commercial  approved in Puerto Rico and Hawaii for this growing season.

In Dec 1999, Gunther Stotsky and colleagues (12) reported that Bt toxin is released into the rhizosphere - around the plant roots in the soil - in exudates from the roots of Bt corn, where the toxin is protected from biodegradation and accumulates.  This raised, for the first time, the question of what is happening underground?   A total of 15 million acres of Bt corn were planted in the US in 1998, 20% of the total acreage. The leaked toxin enters the soil in an activated form - Bt transgenes are truncated to produce active toxin, unlike the precursor-form produced in the bacterium, which has to be cleaved in the gut of susceptible insect pests.  Moreover, the toxin is expressed continuously, and hence exuded for extended periods of time.

In organic farming the toxin is sprayed sporadically in an inactive precursor form, only becoming active in the gut of the target insects once ingested.  Furthermore, it is prayed onto the surface of plants where it is readily biodegraded.   Stotsky suggests that the widespread planting of Bt crops is equivalent to added large doses of active toxin to the soil, not only from the plant root but also from the plant residues after ploughing in, as well as from pollen.  There is at present no clear indication as to how soil communities might be affected by Bt toxin from root exudates.  It may promote selection of toxin resistant target insects.  But receptors for Bt toxins are present in both target and non-target insects, therefore both will be affected.  Bt toxins are active against insects in the Order of Coleoptera (bettles, weevils and styloplids) which contains some 28,600 species, far more than any other Order (13).   The widespread use of Bt genes in crops and the build up of active toxin in the soil will have long term ecologically risks to non-target species and organisms in higher trophic levels, such as birds.

Simultaneously, it was reported that Novartis had filed a patent for another insecticide to be used in conjunction with Bt crops (14).  It turns out that the pest-control spectrum of Bt toxins is limited, and other pesticides have to be used, that have been shown to be very damaging to health.  This completely discredits the industry's claim that Bt is essential for reducing harmful pesticide use.

This April brought further reports on pockets of Bt-resistance among pests in GM fields, and of GM cotton plants turning up as weeds in other crops (15). The cotton boll weevil may make a  come back if such volunteers are ignored. An entomologist at Clemson Univ. said, "I could look across soybean fields and see hundreds of these Bt cotton plants".  A return of this pest to parts of the American Cotton Belt would be a disaster, considering it cost $1.3 million to eradicate them by 1995.

The ecological interaction between organisms is complex and scientifically challenging. The behaviour of insects with regard to choice' of food can have important impacts. This aspect has been overlooked completely in environmental risk assessments of GM crops.  Researchers at Rothamstead in the UK (16) have pointed out that killing non-target species is a risk not unique to GM technology, as conventional regimes actually kill insects in an indiscriminate manner that is equally unsustainable.  They highlight the need to find alternatives to conventional practices and suggest that management and good husbandry of bio-control agents should act in an integrated manner to eliminate caterpillars.

The health assessment of Bt crops relies totally on past experiences with Bt sprays in organic farming.  It is wrong to assume that Bt toxin in GM crops is the equivalent to what has been used for over thirty years on organic produce with no effects.  As with all GM crops, comprehensive feeding trials have yet to be conducted and therefore there is no data supporting the safety of eating Bt crops.  Furthermore, there is a general lack of scientific transparency with all GMOs and Bt-crops are no exception. Crucial data are withheld from the public domain under various confidentiality statements made by the biotech companies in their applications for license.

Leading US Agronomist, Charles Benbrook has just completed a comprehensive review on EPA's management of Bt-corn (17). It provides important insights into the structural and legal shortcomings in the approval process, the major among which was the failure to adhere to the precautionary principle.

The summary of findings reported by independent scientists investigating or evaluating environmental risks are sufficiently compelling to warrant the immediate withdrawal of all Bt crops from use.

Notes and references

1. ISB Environmental Releases Database for USDA APHIS website :www.aphis.usda.gov/bbep/bp/index.html

2. Hilbeck, A., Baumgartner, M., Fried, P.M. abd Bigler, F. (1997). Effects of transgenic Bacillus thuringiensis-corn-fed prey on mortality and development time of immature Chrysoperla carnew (Neuroptera: Chrysopidae) Enivronmental Entomology 27, 480-487

3. Losey. J., Raynor. L., & Carter. M. E., (1999) Nature 399,214 4. See: http://www.ent.iastate.edu/entsoc/ncb99/prog/abs/D81.html [Non-target effects of Bt corn pollen on the Monarch butterfly (Lepidoptera:Danaidae) *L. Hansen, Iowa State University, Ames , IA 50011 and J. Obrycki, Iowa State University, Ames, IA 50011.  Contact e-mail: lrahnsen@iastate.edu ]

5. First Hand Account ^ Industry manipulation of Bt research, by Beck Goldburg, Environmental Defense Fund.  Forwarded to Biotech Activists 11/05/99

6.  The final report of the SAP panel is accessible at <http://www.epa.gov/scipoly/sap/1999/december/report.pdf>

7. Shelton, A.M., Tang, J., Roush, R.T., and E. Earle. (2000)  "Field tests on managing resistance to Bt- engineered plants, Nature Biotechnology, Vol 18;399-342

8. Liu, Y-B., Tabashnik, B.E., Dennehy, T.J.,Patin, A.J., & Bartlett, A.C. (1999) Nature 400:519

9. Huang, F., et al. (1999) Science 284, 965-967

10.   Tanja H. Schuler, Roel P.J. Potting, Ian Denholm, Guy M. Poppy (1999) Parasitoid behaviour and Bt plants.  Nature Vol 400 pp 825

11. Comments Submitted to Docket No OPP-30487a: Registration application for CRY3BB transgenic corn modified to control the corn rootworm  March 20 2000. On behalf of Environmental Defense, the Institute of Agriculture and Trade Policy, the Science and Environmental Health Network, the Center for Food Safety, and the Consumer Policy Institute/Consumer Union.

 12. Deepak Saxena, Saul Flores, G. Stotzky (1999)  Insecticidal toxin in root exudates from Bt corn.  Nature Vol 402 pp 480

 13.  Arnett, R.H., and R.L. Jacques.  Guide to Insects, Simon and Schuster. 1981.

14. Genetically modified plants may still need pesticides, By Andy Coghlan and Barry Fox, New Scientist, 18.12.99

15. Pockets of resistance : A pest might make a comeback thanks to engineered weeds.  New Scientist, By Andy Coghlan April 15 2000.

16.  Poppy, G. (2000) GM  crops:environmental risks and non-target effects, Trends in Plant Scienc 5 , 4-6.

17.Charles Benbrook and Steve Suppan June 2000.  Applying the Precautionary Principle in Assessing Transgenic Corn Technologies in the US.  See <http://www.biotech-info.net/case_studies.html>