1

Introduction

Marijuana, cocaine, and heroin are three of the leading illicit drugs in the world. In 2008, cannabis herb production was estimated at 13,300-66,100 metric tons, and cannabis resin production at 2,200-9,900 metric tons. In 2009, global production of cocaine was estimated to range from 842 to 1,111 metric tons. Potential opium production was estimated at 7,755 metric tons, about 37% of which was projected to be available on the drug market as opium and the remainder as morphine and heroin (UNODC 2010a).

Those drugs are derived from plants: marijuana from cannabis (Cannabis sativa), cocaine from coca (Erythroxylum coca and E. novogranatense), and opium, morphine, and heroin from opium poppy (Papaver somniferum). Illicit cannabis plants are grown in most countries of the world, and it is difficult to obtain reliable estimates of cultivation because they are increasingly grown indoors. The UN Office on Drugs and Crime (UNODC) estimated that 200,000-641,800 hectares of land worldwide were used for outdoor cannabis cultivation in 2008. Afghanistan is the major cannabis producer in the world (see Table 1-1). A survey conducted by UNODC and the Afghan Ministry of Counter Narcotics in 2009 estimated 10,000-24,000 hectares of cannabis cultivation and 1,500-3,500 metric tons of cannabis resin production in Afghanistan. The extent of indoor cannabis cultivation cannot be accurately calculated, but indirect measures indicate that it is increasing because it is less likely to be detected, the yields are higher, and several crops can be grown per year (DOJ 2010; UNODC 2010a).

Illicit coca is cultivated primarily in the Andean countries of Colombia, Peru, and Bolivia. UNODC (2010a) estimated that 232,772 hectares of coca bushes were cultivated in Colombia, 69,925 hectares in Peru, and 37,241 hectares in Bolivia in 2009. Of those estimates, about 68,000, 59,900, and 30,900 hectares of coca bushes, respectively, were harvestable after eradication efforts (see Table 1-2).

The major countries that cultivate illicit opium poppy are Afghanistan, Myanmar, and Mexico. In 2009, the estimated illicit cultivation of opium poppy



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1 Introduction Marijuana, cocaine, and heroin are three of the leading illicit drugs in the world. In 2008, cannabis herb production was estimated at 13,300-66,100 metric tons, and cannabis resin production at 2,200-9,900 metric tons. In 2009, global production of cocaine was estimated to range from 842 to 1,111 metric tons. Potential opium production was estimated at 7,755 metric tons, about 37% of which was projected to be available on the drug market as opium and the re- mainder as morphine and heroin (UNODC 2010a). Those drugs are derived from plants: marijuana from cannabis (Cannabis sativa), cocaine from coca (Erythroxylum coca and E. novogranatense), and opium, morphine, and heroin from opium poppy (Papaver somniferum). Illicit cannabis plants are grown in most countries of the world, and it is difficult to obtain reliable estimates of cultivation because they are increasingly grown in- doors. The UN Office on Drugs and Crime (UNODC) estimated that 200,000- 641,800 hectares of land worldwide were used for outdoor cannabis cultivation in 2008. Afghanistan is the major cannabis producer in the world (see Table 1- 1). A survey conducted by UNODC and the Afghan Ministry of Counter Narcot- ics in 2009 estimated 10,000-24,000 hectares of cannabis cultivation and 1,500- 3,500 metric tons of cannabis resin production in Afghanistan. The extent of indoor cannabis cultivation cannot be accurately calculated, but indirect meas- ures indicate that it is increasing because it is less likely to be detected, the yields are higher, and several crops can be grown per year (DOJ 2010; UNODC 2010a). Illicit coca is cultivated primarily in the Andean countries of Colombia, Peru, and Bolivia. UNODC (2010a) estimated that 232,772 hectares of coca bushes were cultivated in Colombia, 69,925 hectares in Peru, and 37,241 hec- tares in Bolivia in 2009. Of those estimates, about 68,000, 59,900, and 30,900 hectares of coca bushes, respectively, were harvestable after eradication efforts (see Table 1-2). The major countries that cultivate illicit opium poppy are Afghanistan, Myanmar, and Mexico. In 2009, the estimated illicit cultivation of opium poppy 12

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13 Introduction was 128,351 hectares in Afghanistan and 35,787 hectares in Myanmar. After eradication efforts, about 123,000 and 31,700 hectares of opium poppy were harvestable, respectively (see Table 1-3). Estimates for Mexico in 2009 were not available, but estimates from previous years suggest that it maintained its third- place status as in 2008. Other countries in which opium poppy is cultivated in- clude Pakistan, the Lao People’s Democratic Republic, Thailand, Vietnam, and Colombia (UNODC 2010a). The control of illicit-drug use and trafficking is difficult. It involves a va- riety of prevention, control, treatment, and law-enforcement strategies and the participation of local, national, and international government agencies. One ap- proach in these endeavors, eradication of illicit crops, targets the beginning of the drug-supply chain by interfering with crop production in the fields. Crop- eradication measures include aerial application of herbicides, mechanical re- moval that uses tractors or other vehicles to harrow fields, and manual removal and destruction of plants. TABLE 1-1 Major Cannabis-Cultivating and Cannabis-Producing Countries (2008, unless otherwise stated) Cultivated Harvestable Production, metric tons Area, Area, Country Eradication hectares hectares Herb Resin Afghanistan 10,000-24,000 — 10,000-24,000 1,500-3,500 — (2009) (2009) (2009) Bolivia — — — — 1,831 Canada — — — — 1,399-3,498 (2007) Colombia 5,000 — — — 4,000 (2006) (2006) Mexico — 18,562 12,000 — 21,500 hectares Morocco 64,377 4,377 60,000 877 — hectares Netherlands — 1,053,368 — — 323-766 plants Paraguay 6,000 1,838 — — 16,500 hectares South Africa 1,300 1,275 25 — — hectares United States — 7.6 million — — 3,149-7,349 outdoor plants, 451,000 indoor plants Source: UNODC 2010a. Reprinted with permission; copyright 2010, World Drug Report by United Nations Office on Drugs and Crime, Vienna, Austria.

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14 TABLE 1-2 Global Illicit Cultivation of Coca and Production of Cocaine, 1995-2009 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 Coca Bush Harvestable after Eradication, hectares Bolivia 48,600 48,100 45,800 38,000 21,800 14,600 19,900 21,600 23,600 27,700 25,400 27,500 28,900 30,500 30,900 Colombia 50,900 67,200 79,400 101,800 160,100 163,300 44,800 102,000 86,000 80,000 86,000 78,000 99,000 81,000 68,000 Peru 115,300 94,400 68,800 51,000 38,700 43,400 46,200 46,700 44,200 50,300 48,200 51,400 53,700 56,100 59,900 TOTAL 214,800 209,700 194,000 190,800 220,600 221,300 210,900 170,300 153,800 158,000 159,600 156,900 181,600 167,600 158,800 Potential Manufacture of Cocaine, metric tonsa Bolivia 240 215 200 150 70 43 60 60 79 98 80 94 104 113 NA Colombia 230 300 350 435 680 695 617 580 550 680 680 660 630 450 410 Peru 460 435 325 240 175 141 150 160 230 270 260 280 290 302 NA —b TOTAL 930 950 875 825 925 879 827 800 859 1,048 1,020 1,034 1,024 865 a Potential manufacture refers to the amount of 100% pure cocaine that could be produced if all coca leaves harvested in an area under coca cultivation in 1 year were processed into cocaine, on the basis of information on cocaine alkaloid content of coca leaves and efficiency of clan- destine laboratories. Estimates for Bolivia and Peru take into account that not all coca leaf production is destined for cocaine production. b Because of the ongoing review of conversion factors, no point estimate of cocaine production could be provided for 2009. Because of the un- certainty of total potential cocaine production, the 2009 figure was estimated as a range (842-1,111 metric tons). Source: Adapted from UNODC 2010a. Reprinted with permission; copyright 2010, World Drug Report by United Nations Office on Drugs and Crime, Vienna, Austria.

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TABLE 1-3 Global Illicit Cultivation of Opium Poppy and Production of Opiates, 1995-2009 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 Opium Poppy Harvestable after Eradication, hectares SOUTHWEST ASIA Afghanistan 53,759 56,824 58,416 63,674 90,583 82,171 7,606 74,100 80,000 131,000 104,000 165,000 193,000 157,000 123,000 Pakistan 5,091 873 874 950 284 260 213 622 2,500 1,500 2,438 1,545 1,701 1,909 1,779 Subtotal 58,850 57,697 59,290 64,624 90,867 82,431 7,819 74,722 82,500 132,500 106,438 166,545 194,701 158,909 124,779 SOUTHEAST ASIA Lao PDR 19,650 21,601 24,082 26,837 22,543 19,052 17,255 14,000 12,000 6,600 1,800 2,500 1,500 1,600 1,900 Myanmar 154,070 163,000 155,150 130,300 89,500 108,700 105,000 81,400 62,200 44,200 32,800 21,500 27,700 28,500 31,700 Thailand 168 368 352 716 702 890 820 750 — — — — — — — Vietnam 1,880 1,743 340 442 442 — — — — — — — — — — Subtotal 175,768 186,712 179,924 158,295 113,187 128,642 123,075 96,150 74,200 50,800 34,600 24,000 29,200 30,100 33,600 LATIN AMERICA Colombia 5,226 4,916 6,584 7,350 6,500 6,500 4,300 4,153 4,026 3,950 1,950 1,023 715 394 356 Mexico 5,050 5,100 4,000 5,500 3,600 1,900 4,400 2,700 4,800 3,500 3,300 5,000 6,900 15,000 NA Subtotal 10,276 10,016 10,584 12,850 10,100 8,400 8,700 6,853 8,826 7,450 5,250 6,023 7,615 15,394 15,394 OTHER COUNTRIES Combined 5,025 3,190 2,050 2,050 2,050 2,479 2,500 2,500 3,074 5,190 5,212 4,432 4,184 — — 8,600a 7,600a Other — — — — — — — — — — — — — TOTAL 249,919 257,615 251,848 237,819 216,204 221,952 142,094 180,225 168,600 195,940 151,500 201,000 235,700 213,003 181,373 Potential Opium Production,b metric tons SOUTHWEST ASIA Afghanistan 2,335 2,248 2,804 2,693 4,565 3,276 185 3,400 3,600 4,200 4,100 6,100 8,200 7,700 6,900 Pakistan 112 24 24 26 9 8 5 5 52 40 36 39 43 48 44 Subtotal 2,447 2,272 2,828 2,719 4,574 3,284 190 3,405 3,652 4,240 4,136 6,139 8,243 7,748 6,944 (Continued) 15

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16 TABLE 1-3 Continued 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 SOUTHEAST ASIA Lao PDR 128 140 147 124 124 167 134 112 120 43 14 20 9 10 11 Myanmar 1,664 1,760 1,676 1,303 895 1,087 1,097 828 810 370 312 315 460 410 330 Thailand 2 5 4 8 8 6 6 9 — — — — — — — Vietnam 9 9 2 2 2 — — — — — — — — — — Subtotal 1,803 1,914 1,829 1,437 1,029 1,260 1,237 949 930 413 326 335 469 420 341 LATIN AMERICA Colombia 71 67 90 100 88 88 80 52 50 49 24 13 14 10 9 Mexico 53 54 46 60 43 21 91 58 101 73 71 108 149 325 NA Subtotal 124 121 136 160 131 109 171 110 151 122 95 121 163 335 335 OTHER COUNTRIES Combinedc 78 48 30 30 30 38 32 56 50 75 63 16 15 — — 139a 134a Other TOTAL 4,452 4,355 4,823 4,346 5,764 4,691 1,630 4,520 4,783 4,850 4,620 6,610 8,890 8,641 7,754 Nonprocessed — — — — — — — — — 1,382 1,317 2,228 3,698 3,070 2,895 opiumd Potential Manufacture of Heroin, metric tonse Outside 445 436 482 435 576 469 163 452 478 495 472 606 735 724 634 Afghanistan Totalf — — — — — — — — — 529 472 629 757 752 657 a Starting in 2008, a new method was used to estimate opium poppy cultivation and opium and heroin production. The estimates are higher than the previous estimates but of a similar order of magnitude. b Potential production is the amount of oven-dry opium of unknown morphine content that could be produced if all opium poppy cultivated in an area in 1 year were harvested in the traditional method of lancing the opium capsules and collecting the opium gum or latex. c In some countries, poppy straw is used to produce acetylated opium rather than opium gum. However, for reasons of comparability, it was assumed that all opium poppy cultivation is used for opium gum production.

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d These estimates represent the amount of opium that remains opium and is not processed into morphine or heroin. It refers only to Afghan opium because the amount of opium not processed into morphine or heroin in other countries could not be estimated. For years before 2004, no such estimate was available for Afghanistan. e Potential manufacture is the amount of heroin of unknown purity that could be produced if the total potential opium production were converted into heroin, excluding the opium that is consumed as opium and not processed. f This series contains all heroin potentially manufactured worldwide, including heroin and morphine consumed and seized in Afghanistan. The amount of Afghan opium estimated to remain available as opium (potential opium, not processed) is not included in these figures. Abbreviation: PDR, People’s Democratic Republic; NA, not available. Source: UNODC 2010a. Reprinted with permission; copyright 2010, World Drug Report by United Nations Office on Drugs and Crime, Vi- enna, Austria. 17

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18 Feasibility of Using Mycoherbicides for Controlling Illicit Drug Crops Some genotypes of parasitic fungi can infect a single plant species or a small group of closely related species, and the use of these fungal pathogens, or mycoherbicides, formulated and applied in the same ways as chemical herbi- cides, has been proposed as a means of controlling illicit crops. The fungi also have the potential to persist in the soil for many months or years and to affect later attempts to cultivate the crops (see Chapter 3). FUNGAL TERMINOLOGY The terminology of fungi used throughout this report can be confusing to those unfamiliar with the practice of taxonomy (classifying and naming organ- isms) and fungal characteristics. This section presents the names assigned to the fungi under consideration in this report and some of their distinguishing charac- teristics. Organisms are classified with a hierarchical system of categories: king- dom, division (phylum), class, order, family, genus, and species. The Kingdom Fungi is subdivided into phyla. The proposed mycoherbicides considered in this report belong to the phylum Ascomycota. Ascomycota is the largest of the fun- gal phyla, containing more than 60% of described fungal species, including most species of plant-pathogenic fungi. Fungi in Ascomycota may reproduce sexually to produce ascospores or asexually (clonally) by mitotic division to produce a different type of spore, a conidium. Most fungi in Ascomycota require a mating partner to form a zygote (cell formed by the union of male and female sex cells), which then undergoes meiosis (cell division for sexual reproduction) and produce ascospores (Figure 1-1). Some species can self-fertilize to produce a zygote which gives rise to as- cospores (Figure 1-2). Ascomycota organisms that require a partner to complete the sexual cycle are termed heterothallic; those which can complete the sexual cycle without a partner are termed homothallic. The ability of fungi in Ascomy- cota to produce both ascospores and conidia has led to taxonomic complexity because each spore state may have its own name. Thus, a single fungus may be known by more than one name: one name when it produces sexual spores (sex- ual state; teleomorph), and another name when it produces mitotic spores or conidia (asexual state; anamorph). If there are two names, the teleomorph name would be synonymous with the name for the entire fungus (the holomorph). Many fungi in Ascomycota have not been observed to reproduce sexually, al- though they may produce abundant clonal spores (Figure 1-3). In this report, we refer to the proposed mycoherbicides by the species names of the fungi intended for development. A species is commonly denoted by the name of a genus (a group of closely related species) and a species name that serves as an adjective or modifier of the genus name. The proposed myco- herbicides of cannabis and coca belong to the same species, Fusarium ox- ysporum. Some F. oxysporum names are followed by a special form name, or forma specialis (f. sp.) (the plural is formae speciales [f. spp.]), which indicates

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19 Introduction that the fungus appears to infect a specific type of plant species or group of spe- cies. The proposed mycoherbicides against cannabis and coca are F. oxysporum f. sp. cannabis and F. oxysporum f. sp. erythroxyli. (Cannabis and Erythroxylum are the genera of cannabis and coca, respectively). F. oxysporum is known to produce conidia and is not known to produce ascospores, although fungi in many other species of Fusarium are known to reproduce sexually in both hetero- thallic and homothallic manners. Mating Partner Cell and Nuclear Ascomycota Fusion Life Cycle Mitotic Mitotic Diploid Haploid Zygote Spores Mycelium Meiosis Growth Meiotic Spore Spores Germination FIGURE 1-1 Life cycle of a heterothallic Ascomycota fungus. This fungus must have a partner to mate and produce meiotic progeny (ascospores). It can also make mitotic prog- eny (conidia). There could be two names for this fungus: one for the mitotic-spore state (anamorph name) and another for the meiotic-spore state (teleomorph name). Crivellia papaveracea is an example of a fungus with this type of life cycle. Self Fertilizing, no partner needed Ascomycota Lifecycle Mitotic Diploid Haploid Zygote Spores Mycelium Meiosis Growth Meiotic Spore Spores Germination FIGURE 1-2 Life cycle for a homothallic Ascomycota fungus. This fungus does not need a partner to mate and can produce meiotic progeny (ascospores) that are genetically identical to the one parent. If a partner is available, homothallic ascomycetes can also mate to produce recombined ascospores. They also can make mitotic progeny (conidia). There could be two names for this fungus, one for the mitotic spore state (anamorph name) and another for the meiotic spore state (teleomorph name). Brachycladum pa- paveris, which is the asexual form of Crivellia papaveracea, has this type of life cycle.

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20 Feasibility of Using Mycoherbicides for Controlling Illicit Drug Crops The proposed opium poppy mycoherbicides belong to two fungal species: Crivellia papaveracea and Brachycladium papaveris. These poppy pathogens were previously named Pleospora papaveracea and Dendryphion penicillatum, respectively. The changes in names of the poppy pathogens reflect a better un- derstanding of their biology (Inderbitzin et al. 2006); they were found to be closer relatives of Alternaria spp. than of Pleospora spp. (see Figure 1-4). To connect the new names with those of fungi used in older literature, a table is provided in Chapter 5 to document the old and new names for the fungi. When it is unclear which of the two species was studied, we refer to both fungi in this manner: C. papaveracea/B. papaveris. No Known Ascomycota Sexual Cycle Life Cycle Mitotic Mitotic Haploid Spores Mycelium Growth Spore Germination FIGURE 1-3 Life cycle for a mitosporic Ascomycota fungus. This fungus does not ex- hibit a sexual form and only has one name for its mitotic spore state (anamorph name). Fusarium oxysporum has this type of life cycle. FIGURE 1-4 Phylogenetic relationships of Crivellia and Brachycladium species accord- ing to Inderbitzin et al. (2006). Until a species names is proposed for the unnamed Crivel- lia species, it must be referred to as Brachycladium papaveris, which, along with Crivel- lia papaveracea, are the names used for the two opium poppy fungal pathogens discussed in this report.

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21 Introduction STATEMENT OF TASK The Office of National Drug Control Policy Reauthorization Act of 2006 (Public Law 109-469, Section 1111) directed ONDCP to support a scientific study of the use of mycoherbicides in eradicating illicit crops. In response, ONDCP asked the National Research Council to form an expert committee to examine scientific issues associated with the feasibility of developing and im- plementing mycoherbicides to eradicate illicit crops of coca, cannabis, and opium poppy, including an evaluation of the potential human health, ecological, and environmental risks associated with their use and recommendations for the research and development needed for such use. The committee was charged with addressing the following issues about the potential use of naturally occurring strains of mycoherbicides in eradicating il- licit crops: (1) their effectiveness in eradicating target plants; (2) the feasibility of their large-scale industrial manufacture and delivery; (3) their potential spread and persistence in the environment; (4) their pathogenicity and toxicity to non- target organisms, including other plants, fungi, animals, and humans; (5) their potential for mutation and resulting toxicity to nontarget organisms; and (6) fu- ture research and development needed for implementation, such as mode-of- action studies. The specific questions to be addressed are presented in Box 1-1. The committee comprised experts in plant pathology; mycotoxins; fungal genetics, evolution, and ecology; mycoherbicide development, formulation, and application; plant-disease epidemiology; soil microbiology; medical mycology; human toxicology and risk assessment; and ecological risk assessment. This report presents the consensus findings of the committee. COMMITTEE’S INTERPRETATION OF ITS TASK The committee found that some elements of the statement of task were vague and open to interpretation. After discussions with the sponsor, the com- mittee arrived at the following observations and clarifications on how to fulfill its task. Task Clarifications  The term eradication suggested to the committee that complete destruc- tion of the target crop was the intended goal. Discussions with the sponsor made it clear that complete destruction was an unrealistic expectation and that the in- tended goal is substantial control of crop yields by causing disease or weakening a plant’s ability to produce the chemical compounds used to make illicit drugs. However, the sponsor did not specify the desired extent of control of the illicit crops. It was beyond the committee’s charge to determine what an appropriate extent of control would be.

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22 Feasibility of Using Mycoherbicides for Controlling Illicit Drug Crops BOX 1-1 Questions Posed in the Statement of Task Effectiveness:  Are the drug crops (cannabis, coca, and opium poppy) known to be suscepti- ble to the proposed mycoherbicides?  Have the mechanisms of action of the proposed mycoherbicides’ toxicity to illicit-drug crops been established?  Are the proposed mycoherbicides host-plant-specific?  What quantities of mycoherbicides would be needed to eradicate illicit drug crops?  How would the method of delivery affect the effectiveness of the mycoherbi- cides in eradicating the drug crops? Feasibility of large-scale manufacture and delivery:  What sort of facility would be required for the large-scale industrial manu- facture of the proposed mycoherbicides?  What sort of equipment and technology would be required for the delivery of the proposed mycoherbicides on a large scale?  What is the overall technical feasibility of the large-scale industrial manufac- ture of the proposed mycoherbicides?  What consideration would need to be made for large-scale delivery of the proposed mycoherbicides?  What types of field trials of the proposed agents are needed? For example, is testing in tropical or arid environments required? Persistence in the environment:  How long are the mycoherbicides likely to persist in the environment after application?  Do the mycoherbicides have geographic or climatic boundaries?  What combination of environmental conditions (such as temperature, depth in soil, and pH) would favor persistence after application?  What conditions would shorten the persistence of the proposed mycoherbi- cides in the environment?  Could persistence of the mycoherbicides in the environment be controlled? Toxicity to nontarget organisms:  Would the proposed mycoherbicides harm licit crops or kill other soil fungi?  Would the proposed mycoherbicides threaten biodiversity or pose other risks to the environment?  What is the nature of the health risks to animals and humans posed by the use of the proposed mycoherbicides?  What would be the range of transmission of the proposed mycoherbicides and what factors would influence their spread?  Once released, would the pathogens be uncontrollable? (Continued)

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23 Introduction BOX 1-1 Continued Potential for mutation and resulting toxicity to target and nontarget organisms:  What would be the potential of the pathogens to mutate?  Are there environmental or other conditions that would drive mutations in the mycoherbicides?  Does the potential for mutation pose additional risks to nontarget organisms (including other plants, fungi, animals, and humans) or the environment?  How might mutations affect the susceptibility of the target crops to the my- coherbicides?  How might mutations affect the toxicity of mycoherbicides generally? Research and development needs:  Could the effectiveness of the mycoherbicides in eradicating illicit-drug crops be improved through research and development?  What types of expertise would be most relevant for improving the effective- ness and safety of the proposed mycoherbicides?  What types of research and technology would improve the production and delivery of the mycoherbicides?  What type of testing would be needed before mycoherbicides could be safely and effectively used to eradicate illicit-drug crops (for example, mode-of-action studies)?  What would be required under U.S. federal and state laws to test and approve a mycoherbicide of this type, and what guidelines of the International Organisation for Biological and Integrated Control of Noxious Animals and Plants would apply?  Pathogenicity and toxicity are used interchangeably in the statement of task, but they have different meanings. Pathogenicity refers to the ability of a living agent (the pathogen) to infect and cause disease. The affected organism is termed the host. Toxicity is commonly used with two connotations: the capacity of any agent to cause harm to a living organism and the degree or extent of the harm caused by a chemical. In this report, pathogenicity is used to describe the former concept and toxicity to describe the latter concept. The distinction is im- portant because the fungi of interest are competent plant pathogens and are ca- pable of causing disease in the host plants that they colonize, but some also pro- duce chemical metabolites that might adversely affect other plants, micro- organisms, animals, and humans.  Several of the task questions focus on the potential of the fungi to mu- tate. The term mutation often has a negative connotation, so it is important to define how it is used in the report. Mutation refers to change. In genetics, it means a sudden departure from the parental type in one or more heritable char- acteristics. A mutation results in a permanent, heritable alteration in the DNA sequence of a gene or the physical arrangement of a chromosome. Changes in a gene’s DNA sequence can alter the phenotype (an observable physical or bio-

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24 Feasibility of Using Mycoherbicides for Controlling Illicit Drug Crops chemical trait) by altering its expression. Changes in the physical arrangement of a chromosome also could result in new traits even if none of the genes on the chromosome has been otherwise altered. Induced mutations are heritable genetic changes that result from the exposure to chemical and physical agents that are capable of altering DNA or chromosomal structure. Spontaneous mutations oc- cur without known exposure to a mutagenic agent. As used in the statement of task, mutation appears to refer to any stable change in the fungal phenotype that might occur.  The question “What would be required under U.S. federal and state law to test and approve a mycoherbicide of this type, and what guidelines from the International Organization for Biological Control of Noxious Animal and Plants (IOBC) would apply?” is more a legal and regulatory question than a scientific one. The committee did not feel comfortable about developing a “checklist” of testing requirements that must be met, especially inasmuch as regulations vary widely by state and by country. It also was unclear to the committee why the work of IOBC was of specific interest to ONDCP. IOBC is an international pro- fessional society that promotes the development of biological control agents. Although the organization and some of its members were involved in the devel- opment of some international standards for testing pesticides and guidelines for transport and release of biological control agents, it does not have its own set of guidelines. To address the question quoted above, the committee took a broad approach of determining what general types of information would be necessary to test or use mycoherbicides under relevant national or international laws and agreements. Issues Outside the Committee’s Task Determining whether it is feasible to develop mycoherbicides requires de- fining the term feasible. Feasibility clearly encompasses the many scientific and technical questions in the task presented in Box 1-1. However, other issues are critical in determining the feasibility of developing and using mycoherbicides against illicit crops, such as the costs of conducting the research to support the registration of the mycoherbicides, the international procedures for getting my- coherbicides approved for testing and use in different countries, and other eco- nomic, social, and political factors. Evaluating those factors was not part of the committee’s charge. The committee is aware that some researchers have proposed modifying the proposed mycoherbicides genetically to improve their virulence and efficacy in controlling illicit drug crops. However, the committee was asked to restrict its evaluation to naturally occurring strains of the fungi, so genetic modification is not considered in this report.

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25 Introduction COMMITTEE’S APPROACH The committee held three public meetings to gather information to address its task. At the first meeting, on April 20, 2010, the committee met with officials of ONDCP to obtain background on the project and clarification on the scope of work. Representatives of the U.S. Environmental Protection Agency Office of Pesticide Programs gave a presentation on the agency’s experience with myco- herbicides and its requirements for registration. At the second meeting, on June 23, 2010, representatives of the Department of State shared their perspectives on the history that led to the request for the National Research Council study. The committee also heard presentations on research conducted by the U.S. Depart- ment of Agriculture’s Agricultural Research Service on mycoherbicides against coca and opium poppy; on the Forest Service’s struggle to deal with illicit drug crops in national parks and other public lands; on the biological control of witchweed (Striga hermonthica) in sub-Saharan Africa using a strain of Fusa- rium oxysporum; and on the commercial production of mycoherbicides. At the third public meeting, on September 15, 2010, the committee reviewed a poten- tial technique for applying mycoherbicides. The committee heard from other interested parties during the open-microphone sessions at its public meetings and in written submissions. As noted earlier, economic, social, and political considerations in deter- mining the feasibility of developing and using the proposed mycoherbicides were outside the committee’s charge. Such considerations should be taken into account with the scientific factors by any agency or organization that might en- gage in the development of mycoherbicides against illicit crops. To aid in the committee’s evaluation, literature searches were performed to identify relevant research, and ONDCP, the Department of State, and the United Nations were consulted for other relevant, publicly available informa- tion. The committee found that little information on the fungi of interest that could be used to provide well-informed answers to several questions in the statement of task was available. Thus, it answered many of the questions in a broad, qualitative context, drawing from general biological principles and from experience with approved mycoherbicides and related fungi. ORGANIZATION OF THE REPORT The committee organized its evaluation by first providing some context for its review. Chapter 2 provides background on the biological control of unde- sirable plant species. All the mycoherbicides that are approved for use in the United States were developed to combat undesirable plant species. The commit- tee considered general principles learned from developing those mycoherbicides and how they might be applied to developing mycoherbicides against illicit crops. The chapter also discusses issues that are applicable to all the proposed

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26 Feasibility of Using Mycoherbicides for Controlling Illicit Drug Crops mycoherbicides, including pesticide regulation in the United States, international considerations for testing mycoherbicides, and a conceptual approach to evaluat- ing risks to nontarget plants and organisms. Chapter 3 provides a brief overview of the biology and cultivation of cannabis, coca, and the opium poppy. Chapter 4 considers the available data on the Fusarium mycoherbicides that target coca and cannabis and what is known about F. oxysporum in general. A similar re- view of C. papaveracea/B. papaveris is provided in Chapter 5. Chapter 6 pro- vides answers to each of the questions in the statement of task.