Planting Fear: How Real is the Threat of Agricultural Terrorism?

March 4: Workers burn cattle at a farm in Lockerbie, Scotland, in an effort to prevent the spread of foot-and-mouth disease.

Between February 20 and July 114 of this year, 1,844 cases of I foot-and-mouth disease were reported by the British Departía ment of Environment, Food & Rural Affairs, with a smaller number of possible cases reported in France, the Netherlands, and Ireland. As Britain struggled to contain this extremely infectious disease, spread by both direct and indirect contact, an estimated three and a half million cattle, swine, sheep, and goats were slaughtered, and many British farmers faced economic ruin.

This foot-and-mouth outbreak coincides with increasing concern over the potential for agricultural bioterrorism—the malicious use of plant or animal pathogens to cause devastating disease in the agricultural sector. The perception of increased risk stems from recent natural outbreaks (like that of foot-and-mouth and the spread of the West Nile virus in the eastern United States), from an increased focus on “asymmetric” weapons, and in the United States in particular, from heightened worries about domestic terrorism.

Agricultural attack could seem appealing to a broad range of rogue actors, including politically motivated single-issue groups and criminal organizations seeking financial gain. Impacts could be short- or long-term, with a wide range of costs.

One-sixth of the U.S. gross domestic product and one-eighth of all jobs are connected to agriculture, either directly or indirectly. The destruction of crops and/or livestock has a direct financial impact on the grower or breeder, but it also hurts shippers, stockyards, slaughterhouses, distributors, and so on. Attacks may also impact consumers, threatening not only their pocketbooks, but their confidence in the safety of the food supply as well.

Apart from immediate revenue losses, producers may lose future market share if distributors, wholesalers, and retailers choose alternative suppliers. Worse yet, the price of replacing entire crops or herds of livestock—or, depending on the pathogen used in an attack, the need to decontaminate an entire area—could put individual farmers' recovery beyond reach. In addition, seemingly unrelated industries could be affected. For instance, although estimates vary, this year's foot-and-mouth outbreak is expected to cost the British tourism industry at least $5 billion.

Agricultural bioterrorism has received increased attention and discussion within academic, media, and government circles, with most recent studies arguing that agricultural bioterrorism represents a new and dire threat to U.S. national security. 1 But are these studies accurate? Many of their conclusions are pure conjecture, based on worst-case scenarios. Both the threat and consequences of bioterrorism aimed at agriculture remain poorly understood.

However, the threat may not be as dire as alarmists claim, and increased vigilance and institutional reforms could lessen the consequences of either an intentional attack or a naturally occurring disease outbreak.

In the hands of terrorists

There is little empirical data regarding attacks, particularly those by sub-state actors, so analysts and policymakers have been left to discuss the threat based on assumptions about vulnerability. But what, in fact, can we learn based on the motivations of past terrorists?

The “Database of Incidents Involving Sub-National Actors and Chemical, Biological, Radiological, or Nuclear Materials,” maintained by the Center for Nonproliferation Studies at the Monterey Institute of International Studies, lists all terrorist incidents in the last century. It includes 21 incidents that might be classified as examples of sub-state attacks against agriculture. The earliest of these was perpetrated in 1952 by the Mau Mau, a violent nationalist-separatist movement in Kenya, which used a toxin from the African milk bush to kill cattle during their rebellion against British rule.

Most of the 21 incidents were unsophisticated and ineffective, lacking significant impact. Only five occurred in the United States, and almost all attacks were very small scale, involving mostly chemical rather than biological materials. Five attacks were criminal rather than political in nature, and several of the others were purely personal (motivated mainly by revenge). The majority of these incidents might more appropriately be described as product tampering rather than agricultural terrorism.

In 1974 the “Revolutionary Command,” a radical Palestinian group, claimed to have contaminated grapefruit exported from Israel to Italy; in 1978 another Palestinian outfit, the “Arab Revolutionary Council,” targeted Israeli citrus fruit, using liquid mercury as an agent; and in 1988, Israeli grapefruit exports were again threatened with contamination. In 1999 and 2000, Israeli eggs sold domestically were contaminated with salmonella. In this incident, two people died and many others were sickened. Although people had been injured in the earlier attacks on Israeli goods, economic disruption seemed to be the primary goal.

Of the 21 incidents, three hoaxes, three actual incidents, and one ambiguous event involved biological agents. The hoaxes involved foot-and-mouth disease, necrotizing fasci-itis, and an unnamed biological agent. A 1984 threat to use the foot-and-mouth disease virus in Australia, although a hoax, elicited considerable alarm. But there was no evidence that the perpetrator possessed or had access to the virus.

In 1989, there were allegations that a group called the Breeders had released Mediterranean fruit flies to protest the use of pesticides on crops in California. The “Medfly” infestation was particularly damaging to citrus fruit. No one was apprehended in the case, but the number of flies was particularly high in California that year, leading authorities to suspect that some had been deliberately released. But it is impossible to say that the Medfly was used as a terrorist instrument.

It is difficult to extrapolate from such a small number of incidents, but the evidence seems to suggest that sub-state groups and individuals motivated by revenge or financial considerations have been the most likely to use or threaten to use biological agents against agricultural products. The record also shows that these attacks have been low-level efforts with limited impact.

State bioweapons programs

In contrast to what is known about sub-state actors, a good deal of information is available regarding state-run biological weapons programs.

During World War I, German agents infected horses that were being shipped to Europe from the United States, Argentina, and Morocco with glanders and anthrax bacteria. This was accomplished by feeding the horses contaminated sugar cubes or wiping their noses with disease agent. The purpose was sabotage, intended to undermine the Allied war effort rather than to achieve the widespread contamination of livestock. There is no detailed record of animal deaths, suggesting that the attacks were not very effective.

Germany conducted research into plant and animal pathogens during World War II, but it appears not to have used them. Germany also investigated the use of potato beetles and worked on foot-and-mouth virus (including its weaponization) as well as on a range of anti-crop pathogens.

Before World War II, France also experimented with Colorado beetles and researched the rinderpest virus for attack on cattle, but there is no evidence that either agent was ever used. During the war, the United States, Britain, and Canada coordinated their efforts to produce anthrax bacteria for use against German cattle. The British researched foot-and-mouth disease virus, fowl plague bacteria, and pathogens lethal to sugar beets. The United States developed a viral agent to be used against the Japanese rice crop, conducted research into diseases such as the avian Newcastle, rinderpest, and fowl plague, and pathogens directed against rice, potatoes, and wheat. None of these agents were used during the war.

The Japanese biological weapons program during World War II, although most noted for its attacks against the Chinese people, was also directed against agriculture. Japan's anti-agriculture work was based in Manchuria, and to a lesser extent in Southeast Asia. The details of the program remain vague, although it also included research into diseases such as anthrax, glanders, “nose ulcers,” sheep pox, ox plague, and numerous anti-crop agents, directed particularly against certain grains and vegetables. The Japanese used these anti-crop and anti-livestock pathogens in sabotage efforts in Manchuria.

Top: Could California's 1989 Medfly infestation have been a terrorist attack? Above: Wheat plant shows signs of rust fungus.

After World War II, the U.S. agricultural program focused on large-scale production and weaponization of anti-crop agents. By the time the United States unilaterally renounced all forms of biological warfare in 1969, it had conducted research and development on wheat stem rust, rice blast, rye stem rust, foot-and-mouth, rinderpest, and brucellosis (a porcine form was intended to incapacitate humans). As late as the 1950s, the American program's dissemination methods for some anti-agriculture agents involved bomblets filled with an agent-and-feather mix. Later, the American program developed spray systems.

The most widespread effort to develop anti-agriculture pathogens may have been that of the Soviet Union, with agents directed primarily at livestock—foot-and-mouth, rinderpest, and African swine fever. 2 Anthrax and psittacosis bacteria were directed at both livestock and human targets, and pathogens such as wheat rust, rice blast, and rye blast were developed as anti-crop agents. There are allegations from a key Soviet defector that Soviet forces unsuccessfully used glanders in the campaign in Afghanistan in the 1980s, but these allegation cannot be substantiated. The Soviets apparently did not mass produce or stockpile anti-agriculture agents; instead, they maintained the ability to expand production rapidly if desired.

Other states may have considered biological agents as weapons against agriculture. South Africa has been accused of using anthrax bacteria as an anti-animal agent in Zimbabwe in the mid- to late 1970s during the Rhodesian civil war, but the outbreak could also have been a natural occurrence. The Iraqi bioweapons program of the early 1990s included agents like cover smut (an anti-wheat fungal agent) and camel pox. Neither appears to have been mass produced or weaponized. Iraq, however, did weaponize anthrax bacteria, botulinum toxin, and aflatoxins, although details remain sketchy.

Most national efforts outside the United States and the Soviet Union were not technically sophisticated. The German sabotage program of World War I relied on infecting individual horses. The Japanese studied climatic and geographical factors that might affect their use of biological pathogens, but they appear to have made minimal efforts to find effective dissemination techniques.

The technical details

A look at various countries' programs suggests that the development and weaponization of effective anti-agriculture agents is not straightforward—it requires dedicated infrastructure, personnel, and resources.

A successful agricultural attack would require: acquiring and propagating the proper pathogen; processing it for delivery; constructing an appropriate delivery device; and developing a range of techniques to deal with varying meteorological conditions.

No detailed discussion of these factors has been published in the open-source literature, but a determined terrorist could find a great deal of factual information on animal or plant pathogens. Using it to produce a successful disease outbreak, however, would not be straightforward. It would require some degree of scientific sophistication.

Although the United States and other nations place export and/or trade restrictions on dangerous foreign animal and plant pathogens, it is still possible to obtain them from various international laboratories or repositories. 3 Alternatively, pathogens can be isolated from infected animals or diseased crops. Small quantities of pathogens could easily be carried across a customs checkpoint or an unregulated border area, or sent through international mail. Only a few of these pathogens are zoonotic (communicable from animals to humans), so there would be little risk of infection to the carrier. In a globalized society, increased travel by humans and increased transport of agricultural and other goods have already unintentionally spread some pathogens.

The Colorado beetle, or “potato bug,” studied by several countries bioweapons programs

Obtaining a strain of a virus or a fungus does not necessarily mean, however, that it can be used directly as a biological weapon. For example, different strains of the rinderpest virus are immunologically similar, but they vary widely in pathogenicity, lethality, ease of transmission, and host affinity. 4 Such variations, which occur in all animal and plant pathogens, complicate the selection of a weapons-usable strain. In most cases, a terrorist would need the right strain to cause a significant disease outbreak.

Some foreign animal pathogens, like the foot-and-mouth disease virus, are highly infectious and would not need to be cultured—a vial of material might be enough to cause an epidemic. But that is not always the case. Depending on the pathogen, different infective doses would be needed. And infectivity varies even between different isolates of the same viral strain and for different routes of infection (ingestión versus inhalation). If widespread destruction is the goal, moderate or high levels of scientific expertise may be needed to grow, handle, and store larger quantities. Certain parameters involving nutrients and growth conditions would need to be determined experimentally for individual pathogens.

Some animal pathogens are highly infectious and environmentally hardy, so processing—microencapsulation, milling, and drying—might not be necessary. But most plant pathogens and several animal pathogens are sensitive to environmental conditions; protective coatings would need to be applied to increase their survival upon dissemination. Developing such coatings would involve sophisticated scientific skills that are not likely to be available to terrorists. For example, specific microencapsulation techniques used with bio-control agents (fungicides, bacteria) against the Late Blight pathogen have been found to protect potatoes only in local, targeted plots, not over widespread areas. 5

With highly infectious pathogens, there may be no need to develop elaborate delivery devices. Historically, commercially available spray devices have been used in various state-level anti-crop and anti-livestock bio-weapon programs. However, it is easier to deliver a pathogen to cause an epidemic in animals; plant disease epidemics are highly dependent on environmental conditions.

Environmental and meteorological conditions

Both animal and plant pathogens are susceptible to environmental conditions. Infection of crops with plant pathogens would be less dependent on the skill of the terrorist than on specific environmental conditions like temperature and moisture. If the proper weather conditions are not present, typically no plant-disease epidemic will occur no matter how much agent is disseminated. And weather is impossible to control. For example, a 1999 drought in the eastern United States prevented scores of expert university plant pathologists from creating epidemics of the Late Blight disease in research plots—even when growing potatoes that were susceptible and using strains of pathogen that were particularly virulent. 6

Environmental testing would require a dedicated effort involving sophisticated technical expertise and the kind of financial resources that are likely to be available only to state-supported bioweapons programs. The environmental determinants in plant disease outbreaks could be a virtual chokepoint for terrorists trying to utilize potent anti-crop weapons. Although foreign animal pathogens are less sensitive to environmental conditions, many are also vulnerable to temperature changes, sunlight, and disinfectants.

It would be extremely difficult to cause the widespread destruction of a crop because most plants are not grown in isolation. 7 They have already encountered a variety of plant pathogens, and these earlier contacts have increased their resistance. There are only a few cases, such as that of the Late Blight disease that caused potato crop failures in nineteenth century Ireland, where a crop has remained isolated and has therefore been highly vulnerable. There are a few foreign strains of plant pathogens, however, against which current crops have no resistance; some of these pathogens are highly resistant to fungicides. On the other hand, the issue of isolation is more serious in the case of livestock. The United States has quarantined livestock against several foreign animal diseases, making American livestock extremely vulnerable.

All in all, serious technical issues would confront terrorists attempting to launch an “agricultural armaged-don.” But blanket statements on technical feasibility are not sufficient to assess the threat—they must be qualified by examining each of the factors involved in turning a living organism into a biological weapon. In contrast to sensationalist reports on the threat of agricultural bioterrorism, terrorists would face many difficult technical hurdles before obtaining the capability of unleashing this sort of bioweapon.

Prevention

The capability to attack has existed for years, so why have so few attacks occurred? The historical record shows that only a handful of terrorists have used economic targeting and attacks against property.

On the other hand, future terrorist groups may be attracted to agricultural bioterrorism because it may be easier for them to justify the killing of plants rather than people. And it is possible that publicizing the idea of agricultural bioterrorism through sensationalist reporting could promote attacks. Media, academic, and government groups should exercise prudence when discussing this subject in public forums.

As with any act of terrorism, there are political, social, and psychological effects that go beyond those who are immediately affected. For instance, would the use of an anti-agricultural agent increase public fear of direct attacks on humans? And how might political life be affected? Britain postponed national elections and restructured a government agency following the foot-and-mouth disease outbreak. The Ministry of Agriculture, Food, and Fisheries was abolished, replaced by the Department of Environment, Food & Rural Affairs, and the secretary of agriculture was sacked from the Cabinet. In spite of these upheavals, the Labour Party won reelection in June.

Another complication is the difficulty of differentiating between a naturally occurring outbreak and a deliberately induced one. For example, Cuba has repeatedly alleged that the U.S. military has targeted Cuban crops such as sugar cane, tobacco, and coffee with plant pathogens, but it has offered no credible proof that these diseases were anything other than naturally occurring outbreaks.

It is extremely unlikely that any agricultural bioterrorist could fatally wound the entire U.S. agricultural sector or national economy, both of which are strong and diversified. Local, regional, and national effects, however, could be significant. Even to the extent that the United States is vulnerable, it is unlikely that terrorists could strike successfully. An advanced, state-level bioweapons program, however, might be able to overcome or circumvent some technical hurdles. Given the bioweapons programs of Iraq and the Soviet Union, it is possible that state programs might explore agricultural options in the future.

While our examination of open-source historical and technical information demonstrates that the threat of agricultural bioterrorism has been exaggerated, Britain's recent foot-and-mouth outbreak has revealed the devastating effects of agricultural disease outbreaks. In an increasingly globalized society, the potential for more outbreaks can only grow. Given their potential impact, more efforts should be directed at disease prevention and response. Several specific steps should be taken:

Communication among scientists concerned with animal, human, and plant diseases should be increased. Currently, there are limited interactions, linkages, and institutional mechanisms for communication between the public health and veterinary sectors. This problem became apparent during the 1999 West Nile virus outbreak, when the existing surveillance and response structures between public health, veterinary, and other scientific communities failed to appreciate the connection between outbreaks in birds at the Bronx zoo and human cases. 8 In addition, some plant diseases have been found to cause disease in immune-compromised humans. Increased contact and communication could assist in earlier identification of disease outbreaks.

Interaction among veterinarians is frequently limited to concerns with livestock and domestic animals, overlooking the fact that finding diseases in wildlife can serve as an early warning system. Many emerging diseases originate in the wild, and it is important to support increased surveillance and study of disease outbreaks among wildlife populations.

National and international disease surveillance networks need to extend down to the individual farm and facility. Many times, farmers and local veterinarians are the first to deal with and diagnose animal diseases. Since most local veterinarians and farmers will never see a case of foot-and-mouth disease, increased education, from the grassroots to the university level, would increase the prospect of accurate disease diagnosis and rapid response.

Many local and state public health and veterinary laboratory systems are not equipped or structured to allow rapid diagnosis of animal samples. Neither the Centers for Disease Control and Prevention nor the U.S. Army Medical Research Institute of Infectious Diseases is prepared or willing to test animal samples regularly—nor should they necessarily be, considering that they are primarily research facilities. But absent adequate lab capabilities elsewhere, there is currently no alternative. In the face of a massive outbreak of foot-and-mouth or another disease, existing laboratories may be overwhelmed. Additional mechanisms are needed for diagnostics in emergency situations.

Funding for work related to foreign animal and plant diseases should be increased. There is a great deal of funding available for human pathogen research, even for diseases considered extremely unlikely to surface, such as smallpox. At the same time, funding on foreign animal and plant disease has been relegated to the background. Such research, however, offers enormous benefits for U.S. public health.

The Soviet bioweapons program employed hundreds to thousands of scientific specialists devoted to animal diseases like foot-and-mouth and West Nile, as well as expert plant pathologists. Due to restrictions, few U.S. or European facilities and scientists are permitted to work on these pathogens, yet Russia and several other former Soviet republics have unique facilities and scientific expertise. The U.S. Defense and State Departments have been working to redirect former Soviet bioweapons efforts toward the development of medical treatments and other responses to protect against foreign animal and plant diseases. U.S. support and funding for these programs' scientists (administered under the Nunn-Lugar program) should be increased.

Current agricultural practices—the use of monocultures, and intensive livestock production in which animals are closely confined—should be reevaluated. These practices increase U.S. vulnerability to disease outbreaks. Although the costs of making significant changes may be too high, it should be possible to evaluate whether some aspects could be changed in a cost-effective manner.

Additional response structures are needed to address the problems involved in differentiating between natural and intentionally induced disease outbreaks. This might include the formation of objective, independent response teams modeled after the National Transportation Safety Board teams, which investigate catastrophic transportation accidents. These teams could ensure that the investigative process is not cut short or neglected in the face of economic and political pressures to control the outbreak.

Additional research on offensive state bioweapons programs and a strengthened verification protocol for the Biological and Toxin Weapons Convention would also be helpful. Understanding the past and present can help us to better assess future bioweapon threats. Scholarly research on why countries have pursued anti-agricultural bioweapons programs, policies, and strategies, coupled with support for a verification protocol, will make it more costly and time consuming for states to conduct prohibited activities and thus strengthen the international norm against bioweapon development and use.