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APSnet Feature, September 15
through October 31, 1999
Crop
Biosecurity
Prepared by
N. W. Schaad1, J. J. Shaw2, A. Vidaver3,
J. Leach4,
and B.J. Erlick5
1USDA ARS-Foreign Disease-Weed Science Unit,
Ft. Detrick, MD 21702; 2Inst. Molecular Biology and Medicine, University of
Scranton, Scranton, PA; 3University of Nebraska, Lincoln, NE 68583; 4Kansas
State University, Manhattan, KS 66506; 5USDA ARS-Special Interagency Programs,
Beltsville, MD 20705 |
 |
 Abstract
During the 7 - 11 August Joint American and Canadian Phytopathological Society meeting
in Montreal, Canada, the American Phytopathological Society (APS) hosted a symposium
entitled "Plant Pathologys Role in Anti-Crop Bioterrorism and Food
Security." Because of the interest in this topic, we are providing this APSnet
feature article and discussion session as a platform for interested APS members and others
to further discuss and develop ideas to help increase our nations crop biosecurity
and food safety. Over the past several years there has been an increase in new and
emerging plant diseases. Although these diseases are a likely result of natural causes,
instances of deliberate introduction cannot be ruled out. We present references to several
books, articles, and web sites which refer to anti-crop bioterrorism and biowarfare.
Introduction
Agriculture, especially related
to crops, is an extremely important component of the U.S. economy. Crop production can be
negatively influenced to a great degree by numerous factors including crop management,
severe weather conditions, diseases, and pests. Concomitantly, prices
of resulting food products and export |

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| commodities can be negatively
impacted. In addition to natural outbreaks of plant diseases, growers could very well be
faced with deliberate releases of pathogens or pests by individuals, nation-state
terrorists, extortionists, those wishing to influence trading markets or exports, and
others. |
The recent APS symposium on anti-crop bioterrorism
chaired by Dr. Anne Vidaver and sponsored by the Office of International Programs,
Regulatory Plant Pathology, and Bacteriology committees was intended to better educate
plant pathologists and the public about the potential of crop bioterrorism. In his keynote
address, Dr. Tom Frazier stressed the need for government to
address crop bioterrorism issues and for plant pathologists to assist in developing a
science-based defense plan for crops (Dr.
T. W. Frazier, "Bioterrorism and agriculture," see abstract). Several newspaper articles
have been written about the APS symposium including: 1) Columbus Dispatch, (http://www.dispatch.com/news/newsfea99/sept99/bioterr.html);
and 2) Calgary Herald, (www.calgaryherald.com:80/business/stories/990821/2754813.html).
The Calgary Herald article entitled "Crop Warfare Combat Plan Urged" by
Grant Robertson, provides a broad overview of the symposium.
Because of the great importance and interest in the topic,
this feature article has been prepared to provide a platform for interested members and
others to further discuss and develop ideas for dealing with crop biosecurity issues.
Numerous representatives of the administration and congress have publicly registered great
concern regarding the threat of biological warfare (BW) to this country, especially
manifested as bioterrorism. Most recently, in comments that were widely circulated in the
press, Secretary of Defense William Cohen warned Americans of the likelihood of biological
weapons attacks in the coming months and years (www.usembassy.ro/Documents/eur072699105.htm).
One of the most important points made by the Secretary is that being prepared for an
attack which may employ bioweapons of mass destruction is, by itself, a strong deterrent.
| The threat and limited use of
biological agents for warfare and terrorism purposes has a long history. Dr. Wallace Deen
presented a historical perspective of bioterrorism and discussed vulnerabilities in
relation to trends in agriculture (Dr.
W. A. Deen, "A historical perspective of bioterrorism and its implications for North
American agriculture," see abstract).
Several books and articles are available on the subject. A very recent book, Biohazard,
written by K. Alibek and S. Hanelman (Random House, 1999) discussed Dr. Alibeks
experience with the former Soviet Unions extensive BW program. Although Dr. Alibek
referred to the former Soviet Union development of anti-crop pathogens as biological
warfare agents, few details were provided. Alternatively, a more detailed and specific
depiction of the potential of the crop threat was provided by Rogers et al. (1999).
The authors recounted the history of anti-crop weapons |
| as part of the United States program
(disestablished in 1969) and the Iraqi anti-crop weapons effort (developed in the 1980s as
a part of that countrys overall biological weapons program). Demonstrating the
efforts that nations have undertaken to develop anti-crop weapons, the article is as
interesting as it is alarming. |

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| Over the past several years
there has been an increase in new and emerging animal and plant diseases. Examples in the
plant realm include bacterial canker of citrus (Xanthomonas campestris pv. citri),
watermelon fruit blotch (Acidovorax avenae subsp. citrulli), sorghum ergot (Claviceps
africana), Karnal bunt of wheat (Tilletia indica), and |

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scab of wheat (Fusarium graminearum).
The August APSnet feature on "New and
Emerging Plant Viruses" (Damsteegt, 1999) listed sixteen new and emerging viral
diseases including tomato infectious yellows, lettuce chlorosis, and high plains virus of
corn. |
Although the precise causes for the emergence of these diseases are not
known, numerous explanations for these phenomena have been postulated by a variety of
sources. Some explanations include natural causes such as climatological changes, man-made
alterations in certain ecosystems, |
| release of new germplasm, introduction of
contaminated seeds, an increase in international air travel and trade, and so on. However
remote, the possibility that some diseases could have occurred as a result of deliberate
introduction cannot be dismissed. |

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Availability of information on
anti-crop biological warfare (BW) in the public domain
Although few books referencing BW matters mention anti-crop
agents, recent articles and some internet web sites do refer to this subject. A special
issue of Emerging Infectious Diseases published by the Centers For Disease Control and
Prevention (Atlanta, GA), addressed a number of issues, including information-sharing (Kay
et al., 1998), and bioterrorism and public health (Henderson, 1998; McDade and Franz,
1998). The current issue of Emerging Infectious Diseases (vol. 5, No. 4, 1999) is devoted
to BW concerns. However, there is essentially no information concerning crop biosecurity.
Some particularly useful examples of available
information on anti-crop BW include; 1) the web
publication, The Battlefield of the Future (www.airpower.maxwell.af.mil/airchronicles/battle/bftoc.html)
which provides a description of several scenarios in which a foreign country or even
unscrupulous businessmen may wish to employ plant diseases for economic gain (Chapter 10,
Biological Weapons for Waging Economic War); 2) a report by
the Federation of American Scientists that was prepared by The Subgroup on Investigation
of Alleged Use or Release of Biological or Toxin Weapons (http://www.FAS.org/bwc/report.html).
This report covers a number of areas including ideas for strengthening current treaties
and protocols. Appendix III discusses plant diseases and considerations for investigating
a suspected occurrence of anti-crop warfare; 3) a NATO
Advanced Research Workshop entitled "BTWC Security Implications of Human, Animal and
Plant Epidemiology" which was held in the Cantacuzino Institute in Bucharest, Romania
in June 1999. Major topics discussed at this workshop included the need for epidemiology
and disease reporting and methods of outbreak investigation and analysis. This and
other related reports can be found at the University of Bradford, Department of Peace
Studies site, http://www.brad.ac.uk/acad/sbtwc/;
and 4) A microbiology course, taught by Professor R. E.
Hurlbert, includes a chapter entitled "Biological Weapons; Malignant Biology" (www.wsu.edu/~hurlbert/pages/101biologicalweapons.html). While a comprehensive overview of the subject matter is
presented, little is included about crops. A list of over 70 potential biological agents
includes eight plant pathogens (four bacteria, three fungi, and one virus). This
non-validated but provocative site is provided for information only.
While not generally addressing plant diseases
in the context of BW, the world wide web provides numerous resources of accurate and
not-so-accurate information concerning general biological warfare and terrorism. As such,
one should very carefully validate the sources and factual content of all data acquired
through these resources. With this note of caution expressed, one of the most useful
resources is Outbreak (www.outbreak.org/cgi-unreg/dynaserve.exe/index.html).
Outbreak offers comprehensive and detailed online information about emerging diseases and
has a large section on biological warfare issues that provides good background
information, as well as many links.
Recognizing deliberate
releases of plant pathogens
If we are to reduce the potential of deliberate introduction
of crop pathogens, we must be able to fingerprint pathogens and discriminate between
naturally occurring disease events and those which may be deliberately introduced for
harmful purposes. The effective tracking of new and emerging diseases in the U.S. and
throughout the world is critically needed to help make these determinations. An example
whereby molecular fingerprinting has been used successfully to determine the geographic
origin of different strains of a plant pathogen is the tracking of Xanthomonas oryzae pv.
oryzae, a destructive pathogen of rice (J. Leach, "Assuring food security: Detecting and controlling modified
pathogens," see abstract).
Unfortunately, because the international infrastructure concerning plant pathology is not
well developed, the identification of a deliberate release of a pathogen is difficult to
ascertain. A major cause of this deficiency is the absence of a rapid reporting system.
This issue is discussed by R. L. Forster (see
abstract) in his symposium presentation on "Ground Surveillance." To address this problem in rapidly
and accurately reporting diseases, APS has discussed the possibility of supporting
development of a global electronic reporting system to track new and emerging pathogens. |

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There are some excellent
resources for reporting plant diseases and emerging plant diseases on the World Wide
Web. However, these are not designed to address or help identify anti-crop activity and
quality control is an issue. |
A list of plant pathogens
that have been generally considered as potential anti-crop weapons can be compiled from
several sources. One key source is the Australia Group. This informal group, comprising
more than thirty nations including the U.S., was established in the 1980s to try to
control the export of dual-use items and technology for chemical weapons by applying
export licensing measures. In the 1990s controls for human, animal and plant pathogens and
dual-use biological equipment were added. More than a dozen plant pathogens included for
export control by the Australia Group are listed because of their harmful potential if
transferred to nations with biological weapons programs or terrorists. An additional list
of pathogens was provided by Weller et al. (1999) who discussed agents in the context of
biological weapons and the problems that are posed for universities who wish to conduct
research with organisms generally considered to be potential animal or plant weapons
(Weller et al., 1999). Collectively, several plant pathogens believed to be suitable for
weaponization are presented in Table 1. We assess that most of these pathogens have
numerous deficiencies as bioterrorist or BW agents and, as such, may be inappropriate or
too difficult to be used.
Table 1
Disease Agent |
Reference |
| Virus |
|
| Banana bunchy top virus |
AG1 |
| Sugar cane Fiji disease
agent |
Weller et al. |
| Fungi |
|
| Cochliobolus miyabeanus
(Helminthosporium oryzae) |
AG, Weller et al. |
| Colletotrichum coffeanum
var. virulans (C. Kanawae) |
AG, Weller et al. |
| Deuterophoma tracheiphila
(Phoma tracheiphila) |
AG |
| Dothistroma pini (Scirrhia
pini) |
Weller et al. |
| Magnaporthe
grisea/Pyricularia oryzae |
Rogers et al., Weller et al. |
| Microcyclus
ulei (Dothidella ulei) |
AG |
| Monilia rorei (Moniliophthora
rorei) |
AG |
| Phytophthora infestans |
Rogers et al., Weller et al.
|
| Puccinia erianthi |
Weller et al. |
| Puccinia graminis (Puccinia
graminis f. sp. tritici) |
AG, Rogers et al., Weller et
al. |
| Puccinia striiformis (Puccinia
glumarum) |
AG, Weller et al. |
| Sclerotinia sclerotiorum |
Weller et al. |
| Tilletia indica |
Weller et al. |
| Ustilago
maydis |
Weller et al. |
| Bacteria |
|
| Liberobacter spp.
(Huanglonbin or citrus greening disease) |
Weller et al., |
Erwinia
amylovora |
Weller et al. |
| Ralstonia
solanacearum |
Weller et al. |
| Xanthomonas albilineans |
AG, Weller et al. |
| Xanthomonas campestris
pv. citri |
AG, Weller et al. |
| Xanthomonas oryzae
pv. oryzae (X. campestris pv. oryzae) |
AG, Weller et al. |
Xylella
fastidiosa |
AG |
Genetically-modified
micro-organisms. |
AG |
| 1AG,
Australia Group list of plant pathogens.
(http://www.acda.gov/factshee/wmd/bw/auslist.htm). |
|
|
In his symposium presentation on epidemiology and risk prediction, Dr. L. V. Madden
unveiled a probabilistic model for assessing the risk of crop bioterrorism (Dr. L. V. Madden, "Epidemiology and
risk prediction," see abstract). The model includes the probability of
introduction, initial establishment, disease spread, and control. If asked to list the top
10 |
| candidate
plant pathogens with high risk potential for deliberate introduction, most plant
pathologists would probably list those pathogens with which they are most familiar and
have historically caused severe crop losses in the past. Because a deliberate introduction
may involve non-traditional agents or modified agents and might not follow historical
trends, such a decision based on personal experience and history may very well be
misleading. A better approach is to develop criteria and a numerical rating system or
"Effective Pathogen Index" (EPI) to assess risk and probability of harm (N. W. Schaad, "What is an effective
pathogen?" (see abstract). A criteria and a numerical score such
as the following could be developed: |

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Possible
Bioterrorist Pathogen Rating Criteria and Points
| ! |
Produces toxin |
15 |
| ! |
Easy to obtain, handle, and
deliver |
10 |
| ! |
Easy to grow in large amounts |
10 |
| ! |
Highly infectious under many
conditions |
10 |
| ! |
Results in the establishment
of a quarantine |
10 |
| ! |
No chemical control or host
resistance available |
10 |
| ! |
No method for rapid or
reliable detection |
10 |
| ! |
Infects systemically by
natural means |
10 |
| ! |
Spreads quickly by natural
means |
5 |
| ! |
Causes severe crop losses |
5 |
| ! |
Survives long periods and is
persistent |
5 |
A perfect organism would have
a EPI of 10 (for example, add the total points and divide by 10). Similar criteria for a
BW agent as part of a state supported BW program could be developed. These criteria could
include many of the above plus points for ease of genetic manipulation.
To prepare our agricultural
system to withstand a deliberate release of a plant pathogen, a serious evaluation of the
appropriate threat agents must be performed. As stated by Dr. R.
Hickson ("Subtle forms of strategic indirect warfare: infecting "soft"
biological targets; some psychological, economic, and cultural consequences," see
abstract) the psychological, economic, and
cultural consequences of crop bioterrorism, especially attacks on such soft targets as
crop seeds, could have a disproportionally adverse effect on our agriculture and society.
Conclusion
We urge all relevant agencies, to recognize the need to
confront this threat and financially support appropriate research for fingerprinting high
priority pathogens, detecting deliberate releases, developing rapid genetic-based
diagnostic assays, epidemiology and risk prediction, and other scientific and technical
approaches to reduce this risk. It is hoped that this article will stimulate further
discussion of this topic.
Topics on crop
biosecurity that need to be explored include the following:
- Awareness of the problem
- Involvement among plant pathologists
- Collaboration among government agencies, the
commercial sector, international organizations, and universities
- Funding for all aspects of plant pathology
research of significance to crop biosecurity, especially on molecular characterization and
detection and identification of plant pathogens, and air and ground surveillance
instrumentation
Additionally, training in
these areas is much needed for those with responsibilities and interest in all sectors of
crop agriculture including pathology extension specialists, students, crop consultants,
federal and state regulators, and farm advisors at various levels.
Discussion topics
The APS has sponsored a web site for
further discussion of the issues raised herein. Click the link titled in the top
left margin titled "Discussion
Area." Interested readers are urged to examine the
comments posted by others and to post their own thoughts and ideas for the plant pathology
community.
Literature cited
Alibek, K. and S. Hanelman. 1999. Biohazard: The
Chilling True Story of the Largest Covert Biological Weapons Program in the World-Told
from the Inside by the Man Who Ran It. Random House. (ISBN: 0375502319) 336 pp.
Damsteegt, V. D. 1999. New and emerging plant
viruses. APSnet, August 1 to 31.
Henderson, D. A. 1998. Bioterrorism as a public
health threat. Emerging Infectious Diseases (Special Issue) 4:488-492.
Kay, B. A., R. J. Timperi, S. S. Morse, D.
Forslund, J. J. McGowan and T. O'Brien. 1998. Innovative information-sharing strategies.
Emerging Infectious Diseases (Special Issue) 4:465-466.
McDade, J. E. and D. Franz. 1998. Bioterrorism as
a public health threat. Emerging Infectious Diseases (Special Issue) 4:493-494. (http://www.cdc.gov/ncidod/eid/vol4no3/mcdade.htm)
Rogers, P., S. Whitby, and M. Dando. 1999.
Biological warfare against crops. Sci. Am. 280:70-75.
Weller, R. E., C. W. Lyu, C. Wolters, and R. M.
Atlas. 1999. Universities and the biological and toxin weapons convention. ASM News
65:403-409.
Whitby, S. and P. Rogers. 1997. Anticrop
biological warfare-implications of the Iraqi and U.S. programs. Defense Analysis
13:303-318.
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Phytopathological Society
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