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Run, radish, run

Terrorists intent on creating chaos needn't risk hitting cities directly. Bioweapons that attack crops could do just as much damage

Debora MacKenzie

http://www.newscientist.com/hottopics/bioterrorism/bioterrorism.jsp?id=22175000

EVEN when you see it from an aeroplane, the sheer scale of farming in the heartland of North America is hard to comprehend. Each one of those squares or circles in the endless patchwork of maize and wheat, soya and alfalfa that rolls from horizon to horizon can measure a square mile-about 260 hectares, the standard unit for field sizes in this part of the world. Farmers rarely stroll through fields that big. They might send in a sprayer every few weeks, and finally a harvester. Otherwise, plants on which millions depend for food are on their own.

Let us imagine, then, that from your plane you see a small cloud of something emitted from a pickup truck on one of the deserted access roads. You are the only person who saw it. No one notices that the crops have a new infection until harvest. Then the farmer may keep it quiet to protect the value of his crop, or perhaps the infection shows itself only when the crop is eaten, or when next year's seeds are planted. Choose your scenario.

Suppose it was a wheat field and the cloud was spores of a wheat smut. The fungus has little impact on the harvest because US wheat is bred to resist it. But the disease is on the exclusion list of every wheat-importing country in the world. The US loses a billion dollars in exports, there is economic ruin in the wheat belt, world grain prices rise and hunger and unrest stalk some Third World cities.

There again, perhaps it was a maize field, and the cloud was millions of whiteflies carrying a usually harmless maize virus that has been genetically engineered to make botulinum toxin. The toxin turns up in beer made partly with maize, and sickens some people. Next year, more maize is affected as local whiteflies acquire and spread the virus. Another food scare. Another government's credibility in tatters. The US launches a billion-dollar whitefly control programme and burns thousands of hectares of farm land.

Or it could have been a soya bean field, and the cloud was an aerosol of Pseudomonas tabaci-a bacterium that produces deadly tab toxin. Relatively few fields are affected, but soy is used throughout the food industry. The contaminated batch kills some cattle, then a few people. Too small an outbreak to count as a major threat to public health, but enough to fuel a massive food scare. US soya exports grind to a halt. World fodder and meat prices skyrocket.

Killing fields

Improbable scare stories? That depends on who you ask. Crop bioterrorism may not have made it on to the agenda in Europe, but a growing band of plant pathologists and defence analysts in North America claim that if your aim is to wreak economic damage, destabilise governments, or simply get a business advantage, there are few easier targets than those lonely waves of grain. No one is claiming that such attacks have already happened-although that has not been ruled out. But at a symposium on anti-crop bioweapons at the Joint American and Canadian Phytopathological Society meeting in Montreal in August, they argued that measures must be taken now to stop bioterrorist strikes against crops becoming inevitable.

Crop diseases are not a new temptation. By the time the US renounced biowarfare in 1968, it had stockpiled 30 000 tonnes of wheat stem rust spores to drop on the Soviet Union, and a tonne of rice blast for Asia. The Soviet Union stockpiled wheat stem rust, and pathogens of maize and rice. Iraq had a wheat smut bomb.

But what has changed is the objective of crop biowarfare and the ease with which a "biobomb" might be deployed. The military motive has traditionally been to deprive an enemy of food during wartime, says Mark Wheelis of the University of California at Davis, who studies bioweapons for the Federation of American Scientists in Washington DC. This goal was so difficult to achieve, he says, that it helped convince the US to abandon crop weapons research when it did. Terrorists, on the other hand, don't need to annihilate the whole harvest to disrupt trade or discredit authorities. If that's the goal, a little plant disease-or the rumour of it-goes a long way.

Even in rich countries the average city has only enough food to last five days, writes Wallace Deen, a consultant formerly with the US biological defence programme, in a report published in November in the Annals of the New York Academy of Sciences. In poor countries, a slight reduction in harvest can raise staple food prices for the urban poor enough to spark civil disturbance. Witness Indonesia after the Asian financial crisis in late 1997-relatively small price rises for rice fuelled food riots in major cities around the country.

Health scares might be a better way to destabilise governments in the wealthy West. At the Montreal symposium, "everyone thought it significant that it only took a little bit of dioxin in Belgium last summer to create a food scare, ruin the livestock industry, destroy food exports and bring down the government," says Norm Schaad, of the Foreign Disease and Weed Science Unit in Fort Detrick, Maryland, part of the US Department of Agriculture (USDA). "A terrorist might do the same with only a small outbreak of the right crop disease."

Political or ideological enemies needn't be the only targets-rivals for export markets may also be tempting. China, a major maize exporter, would benefit if disease blighted US maize, and vice versa. Even corporations could get in on the act. "Say one company grows pineapples in countries where production is limited by a pathogen, which does not occur in countries where a rival operates. The first company might even out this trade advantage by spreading the pathogen," says Wheelis.

"The globalisation of trade is the most important development for those who would use biological weapons against plants," says Deen. Bioterrorists can cause havoc, he says, by contaminating just a fraction of a crop-international trade restrictions will do the rest.

Under the World Trade Organization's "phytosanitary" rules, a minor disease outbreak can take an entire crop off the export market. Take karnal bunt, a relatively mild-if highly infectious-wheat smut that turns grain black, sticky and inedible. When the smut blew into Arizona from Mexico two years ago, 32 countries, including China, banned US wheat imports in one day. The US spent hundreds of millions of dollars to eradicate the fungus and save its $5 billion annual wheat exports. This episode helped to fuel current US fears of anti-crop weapons, as it dawned on plant pathologists that a deliberate attempt to sabotage US grain exports might not look very different.

So much for motives, but what about means? Building a biobomb aimed at plants would be a far less ambitious undertaking than designing one to take out humans ("All fall down," New Scientist, 11 May 1996, p 32). A large-scale biological attack on people needs a carefully "weaponised" germ, to ensure that pathogens normally spread by close physical contact can be transmitted through the air and still be infectious. Plant viruses, bacteria and fungi, on the other hand, are already adept at seeking out and destroying victims that don't move. They are conveniently adapted to be spread by the wind and insect vectors.

And although genetically engineered crop bioweapons may sound scary, there's little need for them. "You can always find a natural plant pathogen as nasty as anything you could create," says Anne Vidaver, head of the Center for Biotechnology at the University of Nebraska, Lincoln. One exception might be an otherwise benign virus engineered to produce a human toxin-harmless for the plant, but a nasty surprise for whoever eats it.

Naturally occurring fungi such as smuts and rusts are far more likely to be a crop bioterrorist's weapon of choice, says Vidaver. Fungal spores are tough, and can infect crops in a wider range of growth stages and environmental conditions than most bacteria and viruses. Fungi can also produce potent toxins, so even a small infestation can make an entire harvest toxic.

Pathogens for plant bioterrorism are a lot less trouble to breed than those aimed at humans because they need not be highly specific to the target, or even destroy that much of a crop to have an impact. Just a small greenhouse full of the crop and a few pathogens collected from local crops-which are likely to be different from those to which the crops in your target country are immune-would suffice. A plant biological weapon would even be safer to manufacture than one designed to attack humans, which can always turn on its creators.

All the same, preparing a crop biobomb would not be a trivial undertaking. For instance, the spores would have to be specially formulated to prevent clumping, and to protect them from ultraviolet light. But with a little luck and a little technical expertise, a weapon could be cooked up in someone's backyard.

They could even get away with it. Spray anthrax from a light aircraft over bustling Washington DC and someone is going to notice. Spread spores of karnal bunt over the lonely plains of Kansas and in all likelihood nobody will see. Agriculture may be the world's biggest industry, and the most vital for human well-being, but it is also one of the least secure. "You could do enough damage to achieve your goal just by bringing in a suitcase full of vials of the pathogen and strolling past a field with an atomiser," says Wheelis.

Soft target

What's more, natural outbreaks of novel plant diseases have multiplied dramatically over the past decade as food, seed and people cross borders at ever-increasing rates. In North America, 25 plant viruses alone are listed as new or re-emerging, while the European and Mediterranean Plant Protection Organization in Paris has an "alert list" of 31 fungi, bacteria and viruses that are threatening to invade Europe. "With all these novel infections happening naturally," says Vidaver, "it may not be obvious if an outbreak is deliberate."

One way to deter would-be bioterrorists is to deny them deniability. "If we could say where a pathogen comes from, we could narrow things down," says Schaad. To that end, his unit at the USDA has collected thousands of plant bacteria from around the world. The next step is to DNA fingerprint the bacteria so that when a suspicious outbreak occurs, plant pathologists will quickly be able to work out where the errant pathogen came from. There are no libraries for fungal and viral pathogens. "We spends millions collecting genetic varieties of crops, but nothing on collecting their pathogens," says Schaad.

In September, President Bill Clinton announced that $215 million would be spent to upgrade a USDA agricultural quarantine laboratory on Plum Island off the coast of New York State, to deal with threats to US agriculture, including plant pathogens. The lab will be equipped to analyse pathogens sent in from any suspicious outbreak. Assuming, of course, that someone notices such an outbreak in the first place. Farmers are not obliged to notify the authorities when an outbreak occurs. An attack "could occur without us knowing it, because we really don't have the tools in place to detect [it]", Floyd Horn, head of the USDA's research service, told the US Senate last month.

"We need automated systems that will enable people to get immediate identification of pathogens in the field," says Schaad. Such systems would rely on DNA and protein analyses similar to those being developed to detect biological weapons aimed at people ("Bioarmageddon", New Scientist, 19 September 1998, p 42).

No amount of technology will help, of course, if there are not enough plant pathologists to police the crops. Even as the threat of natural and unnatural disease outbreaks increases, says Bob Forster of the University of Idaho in Kimberley, there is a declining number of people who can identify diseases in the field.

Assuming you have identified a crop bioterrorist attack, how do you limit the damage? Fungicides can stop or slow the spread of a fungal disease. But for crops infected with bacteria or viruses, usually the only option is to burn them, and eradicate any insect vectors, which can be extremely difficult and costly.

An alternative approach would be to rapidly replace contaminated crops with those that are resistant to the pathogen. Plant breeding companies are investing millions characterising plant genes. In a few years, when a new disease strikes, it may well be possible to pull out the right resistance gene and breed it into the crop that is under attack. The USDA has already identified 26 genes that protect against the barley stripe rust that was wiping out the crop in the northwest of the US in 1995. But it takes resources and time to breed new characteristics into crops and get them out to the farms, so this line of defence will only be available to the wealthy West, and at best can only reduce long-term damage. Consumer opposition to genetically modified crops could also make this approach uneconomical.

Nor is there any guarantee that there will always be a resistance gene available. Take wheat streak mosaic, a virus that is spreading in North America and can cause catastrophic crop losses. Despite extensive research, no one has ever found a resistant variety. Alternative strategies do exist-such as using genes from other species-but ultimately any attempt to engineer resistance into plants only works until bioterrorists find a new pathogen. With such strike and counter-strike, "the world could get itself into a bioweapons arms race", warns Brian Halweil of the Worldwatch Institute, an agricultural and environmental think tank in Washington DC.

According to Vidaver, the best strategy is to reduce the threat of crop bioterrorism in the first place. This goal, she says, can be achieved in part through limiting the spread of infections by abandoning the uniformity of modern farm fields in favour of diverse plant varieties and more crop rotation. Modern American farms, with their huge expanses of one variety of wheat, maize or alfalfa, are "a disaster waiting to happen", she warns.

With the ever-increasing threat of natural plant diseases, investing in improved vaccines and disease diagnosis, and a move away from monocultures could start to make good economic sense. The irony will be if North American fears of crop bioterrorism force its farmers to adopt methods that coincidentally give it more of an edge over its global competitors-even if the terrorists never strike.


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