It’s a good idea to look critically at any powerful new technology, and the creation of genetically-modified organisms, GMOs, is no exception. Like any new technology, it might have unanticipated, deleterious consequences that outweigh any benefit. Many criticisms of GMO have of course been raised, as a brief interrogation of the internet will show. But unfortunately, the criticisms of GMOs we hear most often are not the most important ones, and the ones that are most important are often not heard clearly. Most of the criticisms on the internet do not represent objective, valid criticisms; most often they are a reflection of values.

Warning

If you believe that under no circumstances should genes from one organism be introduced into another, please read no further (I’m thinking of you, Greenpeace). If you think that either (i) scientists are in collusion with industry to push the GMO agenda even though they know it’s harmful to humans and the rest of the environment (i.e. scientists are evil), or (ii) scientists don’t understand the science of GMO, or the risks it poses (i.e. scientists are ignorant), or both, please read no further. This article is meant for readers who don’t hold those value judgments. There are plenty of other web sites that will indulge the rest of you. Thank you.

For those still with me, here is today’s lesson: GMO is much more complex than Greenpeace, or Monsanto, try to tell you. Every project needs to be examined in granular detail to determine whether the benefit outweighs the risk. Let’s look at a few cases.

Clean medicine and a useful outcome

Genetic modification using the tools of molecular biology, described by the term “genetic engineering” (GE), began in the science of microbiology. It arose from an interest in antibiotic resistance, which is a clear and present danger to human health. By the 1970s it was known that drug resistance often arises from genetic elements that can be transferred from one bacterium to another (“horizontal gene transfer”). These elements are located on short, usually circular, DNA elements called plasmids. Given their ability to shuffle between bacterial cells, molecular biologists wondered whether plasmids could also be used to shuttle other genetic bits into living cells.

Indeed they could. The result was, among other products, pure human insulin produced in yeast or bacterial cells in unlimited quantities, and human growth hormone (HGH) free of contamination by the deadly, untreatable, vector of Creutzfeldt-Jakob disease (CJD) (previously, HGH could only be obtained from the brains of human cadavers, the occasional one of which carried the deadly CJD). These were positive outcomes. But their development only happened after a serious look at potential biohazards of GE. The concerns were raised by the scientists involved in the work. After a great deal of deliberation and testing, rules for safe microbiological GE were laid down and the work commenced. The experience since has justified the decision to go ahead.

Clean medicine, but an undesirable outcome

The ability to produce Human Growth Hormone has some useful applications, as well as some unapproved ones, such as trying to reverse the effects of ageing. It therefore seemed reasonable, in the 1980s, to think that animal homologs might be useful in agriculture. For example, it has been known since the 1930s that BGH, bovine growth hormone, increases milk production in dairy cows by 12-16%. So Monsanto created BGH made from recombinant DNA in bacteria, rBGH (trade name Prosilac). rBGH does, indeed, increase milk production in dairy cows. But two kinds of concerns about its use have come up. The first, which is not well supported, but is a subject of debate, is that it might present a danger to those drinking the milk. Most studies have concluded that such dangers are probably non-existent or very small, but further work is needed.

The other concern about the use of rBGH is its harmful effects on the health of the cows, as reviewed by a meta-analysis of existing research in 2003 (1). The peer-reviewed results of such studies indicate that rBGH increases clinical mastitis in the cows by 25% and the likelihood of becoming lame by 55%, among other symptoms. (Bovine clinical mastitis involves inflammation and pain of the mammary gland and udder, and the appearance of clots or pus in the milk. Not nice.) Results such as these were the basis on which the European Union banned the use of rBGH (altogether some 27 countries, including Canada, have joined that ban; the US is an exception). This is an example of unintended consequences of GE.

Bt toxin in agriculture

A lot of cotton grows in India — only China produces more. One of cotton growers’ biggest problems is an insect pest called the cotton bollworm. Corn in Europe and North America is subject to a similar pest, the European corn borer. For many decades, growers have sprayed a product called “Bt toxin” on their corn, which protects it against the corn borer. Bt toxin is named after the bacteria that produce it, Bacillus thuringiensis. B. thuringiensis in turn is named for the state of Thuringia, in Germany, where it caused a disease outbreak in flour moths in 1911 (it was actually first identified ten years earlier when it produced an infection of silk worms in Japan). The Bt toxin produced by these bacteria kills insects that ingest it by destroying the integrity of their gut cells.

Dried extracts of B. thuringiensis containing the Bt toxin have been sprayed onto corn to control the corn borer for decades. The commercial product began to be used in the United States in the 1960s, but it was used in Europe for decades before that. Bt is considered safe and innocuous for mammals, and it is allowed in organic agriculture. Because of widespread spraying, the Bt toxin protein is detectable on many kinds of fresh food in the supermarket, including crops on which it is not used. Everyone has been exposed to Bt toxin.

Different strains of B. thuringiensis produce different toxins, with different targets; in one case Lepidoptera (butterflies and moths), in others, flies, beetles, wasps and bees, and in still others, nematodes. It is without effect on mammals because the protein made by the bacteria is a “protoxin,” an inactive precursor of the toxic form. In the relatively alkaline conditions of the gut of the insect larva, the protoxin is converted to the toxic form by an enzyme, resulting in death. The guts of mammals, including humans, are acidic, and do not activate the protoxin; there are no known cases of Bt toxicity in animals.

A shortcoming of spraying Bt is that the toxin can only kill insects that attack the outside of the plant. But much of the damage is caused internally, during the larval stage of the corn borer, and is not prevented by spraying. In addition, the toxin is destroyed by UV light, and doesn’t have a long half-life in the sun. Multiple applications during the growing season are required for maximum effect.

To make Bt more effective, the gene for the Bt toxin has been introduced into the genomic DNA of corn. Initially this was done by the “gene gun” (biolistic) method, and since the mid-1990s, by fusing it into a delivery plasmid derived from another bacterium, Agrobacterium tumefaciens. Each type of Bt protein is specific; it will attack and kill a limited number of kinds of insects. The one used in corn, delta-endotoxin, targets the larva of the European corn borer. The production of Bt toxin inside the cells of the corn plant protects it against the corn borer more efficiently than spraying. Over 40 million hectares (100 million acres, over 80%) of the corn grown in the United States contains the Bt gene, and some European countries allow its use, even though they forbid any other GE crops for human consumption. Bt corn is safe and economically useful.

A slightly different Bt gene, specifically targetting the cotton bollworm, has been inserted into cotton, which protects it against the cotton bollworm. Millions of acres of “Bt cotton” are grown around the world. But there have been some scary stories related to its use.

 Thousands of dead sheep

A story that illustrates the issues surrounding Bt cotton concerns sheep in India. In particular, several thousand sheep that were said to have died in 2006. That number has been reported to be as high as 10,000. They died within days of eating “Bt cotton.” There is a sad YouTube clip of a distraught Indian farmer who lost sheep due to Bt cotton here.

The deaths of huge numbers of sheep due to Bt cotton has actually never been documented; they are more of a “rural myth.” After the 2006 “outbreak”, a vet carried out autopsies on four or five dead sheep and concluded that the animals may have been poisoned by ingesting a chemical insecticide. Stories were collected from shepherds who had lost sheep, and the larger story continues to be reported on the web — for example, here. But direct tests of the toxicity of Bt proteins by agricultural experts found no hazard at all. When Bt cotton was tested before approval in India in 2002, an Indian seed company conducted multiple field trials and carried out nutritional studies and concluded it was safe. Another study was conducted in an independent lab in Lucknow, India, in 1998, and also found no danger to animals. Investigation at a College of Veterinary Science in Hyderabad, India, in 2010, reached a similar conclusion: Bt cotton presents no hazard to sheep (2). Moreover, although about 90% of the cotton produced in India carries the Bt gene, there have been no reports of such events before or after 2006. The data against Bt cotton being dangerous is summarized here.

A suicide epidemic in India

A much more sinister story then developed, related to Bt cotton in India. It began in 2011, when an American filmmaker, Micha Peled, released a documentary titled “Bitter Seeds,” which argued that Monsanto and its seeds are responsible for the suicides of hundreds of thousands of farmers in India. Food guru Michael Pollan lauded the film, as did the celebrity chef Alice Waters. In 2013, an article in Al Jazeera Online furthered this story. The article was written by the charismatic Indian ecologist and activist Vandana Shiva, and the story of Indian farmers’ suicides has subsequently grown into a legend. She emphatically stated that the reason for the suicides was that Monsanto’s Bt cotton seeds have become ever more expensive, and that they had failed to deliver on their promise. Many farmers, burdened by debt from the purchase of seed, and then getting no crop to repay the debt, chose suicide because they saw no way to continue. In an ironic touch, her article in Al Jazeera said that many of the farmers committed suicide by drinking Monsanto pesticide.

The story has been propagated, particularly by Western liberal spokespeople like Bill Moyers and Bill Maher. The Stanford biologist Paul Ehrlich, author of the 1968 classic The Population Bomb, and a member of the National Academy of Sciences, stated that Monsanto had “killed those farmers in India.” Shiva has become an international celebrity for her anti-globalization and anti-GMO views, which include the opinion that Monsanto is an evil influence on Indian agriculture, and is directly responsible for the huge number of Indian farmers committing suicide (she uses the word “genocide” freely). She has been awarded honorary doctorates at several universities, and international prizes for her work. Her followers on social media are legion. The Guardian named her one of the top 100 most inspiring women in 2012. Prince Charles, a vocal critic of biotechnology, keeps a bust of Shiva on display (the activist, not the Hindu God). But some of her claims are astonishing. For example, in a speech Shiva has said of Monsanto that “now they control the entire scientific literature of the world.” Nature, Science, and Scientific American, three widely admired publications, “have just become extensions of their propaganda. There is no independent science left in the world.”

A second look at those suicides

The number of suicides in India is estimated to be about 175,000 per year (WHO), and the number of farmers committing suicide since the mid-1990s is about 10% of that number. In some states, farmer suicides accounted for as much as 15% of the total. (This in itself is curious, since farmers are estimated to comprise about 24% of the population of India; they appear to be highly underrepresented among suicide victims.) While any number of suicides is tragic, the distribution of these suicides suggests a different cause, not Bt cotton. The suicides occurred mainly in 5 of India’s 28 states. Some states with high agrarian suicide rates do not have cotton farmers, and suicides among farmers were virtually absent in 10 states in which cotton is an important crop. The areas of the country with high levels of farmer suicides do not correspond to those heavily planted in cotton. The agricultural economist Anoop Sadanandan (3) has investigated the factors related to the suicides, and has indeed found a correlation with financial stresses. But not related to Bt cotton or Monsanto, rather, to credit crises among farmers that are related to financial reforms. These reforms were carried out in certain states, and made it more difficult for small farmers to obtain credit from banks and other institutions. As a result, they borrowed from private lenders, at exorbitant rates. According to this study, there were few suicides in states where farmers had good access to institutional credit and farm insurance.

The New Yorker science writer Michael Specter went to India at the behest of Dr. Shiva to investigate the subject of suicides of farmers. In the resulting article (here) (Shiva’s response to Specter’s article is here), he heavily criticizes Shiva’s position. He noted that “Most farmers I met in Maharashtra seemed to know at least one person who had killed himself, however, and they all agreed on the reasons: there is almost no affordable credit, no social security, and no meaningful crop-insurance program.” Moreover, the Indian farmers he talked to said that before Bt cotton, they would have to spray frequently, and it would make them sick (actually it was the women who did most of the spraying).

Other parts of the story from the anti-GMO advocates are also not well supported. For example, the claim the Bt cotton had failed. It is true that at the beginning of their use (around 2002), the great popularity of Bt seeds quickly attracted counterfeiters who sold fake seeds to the farmers, and these indeed failed. Many people suffered, but this crime has since been shut down. In contrast to stories of the failure of Bt cotton, in 2012 the Indian minister of agriculture stated that the country’s production of cotton had increased by 65% since 2002. Some of this increase may have been due to other factors, but still, there’s no evidence of the failure touted by critics like Shiva. Another factor to consider is that suicide rates among Indian farmers began increasing before the introduction of Bt cotton (4), although they have continued to increase since.

As for the claim, by Greenpeace, Shiva, and others, that Indian farmers are compelled to buy Bt cotton seeds from Monsanto, that isn’t correct. They have a choice (Bt, or non-Bt), but have overwhelmingly (90% or more) chosen the Bt seeds because they see that they can produce higher yields. And they are free to plant their harvested seed — the presence of a “terminator gene” in Monsanto Bt cotton seeds is a myth. In fact, the Farmers’ Rights Act of 2001 guarantees every person the right to “save, use, sow, resow, exchange, share, or sell” his seeds. Shiva is well aware of that guarantee, since she is proud to claim partial credit for having it passed. Most farmers, though, prefer to purchase their seed, whether Bt or not, from commercial suppliers because it’s of higher quality. But some farmers do save and replant, and in some cases have crossed the Bt trait into other strains of cotton.

It’s complicated

But the existence of valid criticism of the anti-Bt cotton thesis doesn’t mean that wholesale adoption of Bt cotton is necessarily a good idea. There is a complexity that isn’t clear from reading the literature of either Greenpeace, Shiva, or Monsanto. According to a careful analysis (4), Bt cotton has value only for cotton grown under irrigation. Rain-fed cotton growers harvest one crop a year, and the timing of their crops and the emergence of the cotton bollworm is such, that the plants are not attacked — their period of susceptibility misses the infestation period of the insects. These farmers tend to be among the poorest, and their expenditure on the (admittedly more expensive) Bt cotton seed can impoverish them, especially if they borrow from usurious lenders to plant their crop, or the crop fails for other reasons. According to Gutierrez et al. (4), ” . . . the costs of the Bt and insecticide technologies decrease with increasing yield making it an acceptable assurance option in high-yield areas, but not in areas with low yields with high variability where the high costs increase the risk of bankruptcy (and suicide).” And in at least some states, it is precisely these smallholders who have lost access to institutional loans.

It may well be the case that subsistence farmers, especially in areas with low but highly variable yields, cannot afford the high costs of industrial farming technologies that can contribute to their indebtedness, and in some cases, suicide.

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Footnotes

1. Dohoo, I. R., L. DesCoteaux, K. Keslie et al., A meta-analysis review of the effects of recombinant bovine somatotropin. 2. Effects on animal health, reproductive performance, and culling. Can. J. Vet. Res. 67 (4) 252-264.
2. Anilkumar, B., A. G. Reddy, B. Kalakumar, et. al., Sero-biochemical Studies in Sheep Fed with Bt Cotton Plants. Toxicol Int. 2010 Jul-Dec; 17(2): 99–101.
3. Sadanandan, A., A. Political Economy of Suicide: Financial Reforms, Credit Crunches and Farmer Suicides in India. The Journal of Developing Areas. 48 (4) 287-307, 2014.
4. Gutierrez A. P., L. Ponti, H. R. Herren, J.  Baumgärtner and P. E. Kenmore. Deconstructing Indian cotton: weather, yields, and suicides. Environmental Sciences Europe2015, 27, 12. URL: https://enveurope.springeropen.com/articles/10.1186/s12302-015-0043-8