Agriculture, Methyl Bromide, and the Ozone Hole: Can We Fill the … · 2020. 9. 23. · have occurred (64). The ozone holes of 1992 and 1993 were the most severe on record (24,77)

964 Plant Disease / Vol. 81 No. 9

Jean Beagle RistainoDepartment of Plant Pathology, North Carolina State University, Raleigh

William ThomasStratospheric Protection Division, Office of Atmospheric Programs, United States Environmental Protection

Agency, Washington, DC.

!GRICULTURE��-ETHYL�"ROMIDE�AND�THE�/ZONE�(OLE

#AN�7E�&ILL�THE�'APS�ethyl bromide is a widely usedfumigant in U.S. agriculture and isone of the five most used pest-

icides in the United States (68). Between25,000 and 27,000 t of methyl bromide areapplied annually (70). More than 75% ofthe use of methyl bromide is for preplantfumigation of soil (68) (Fig. 1A). Inaddition, methyl bromide is used forpostharvest treatment of nonperishables(13%) and perishables (8.6%), and forquarantine purposes (<1%). The compoundalso occurs as an intermediate in chemicalmanufacturing and is used as a medicalsterilant. Methyl bromide is an effectiveherbicide, nematicide, insecticide, andfungicide and has been used commerciallyin the United States for soil fumigation andquarantine purposes for most of thetwentieth century (53).

Considerable evidence has accumulatedthat methyl bromide is a potent ozone de-pletor, and the compound is scheduled tobe phased out in the United States by 2001under the Clean Air Act (71). The use ofmethyl bromide was a critical factor indramatic changes in crop production sys-tems in California, Florida, North Caro-lina, and elsewhere. Crop rotations wereonce standard methods of pest manage-ment before widespread use of soil fumi-gation and plastic mulching. Production ofcrops such as strawberries and fresh mar-

ket tomatoes has become highly dependenton methyl bromide use, leading to reduc-tions in crop rotation and in diversificationof production practices (7). The economicviability of specific crops in Florida, Cali-fornia, North Carolina, and other statescould be affected by the loss of this com-pound if no alternatives are available(9,62,69). The purpose of this article is toreview the scientific, trade, regulatory, andpolicy issues that will affect the use ofmethyl bromide in agriculture and to dis-cuss methyl bromide alternatives.

Is There an OzoneDepletion Problem?

Ozone is a rare form of oxygen con-taining three atoms per molecule (O3) andis highly reactive. Most ozone is found inthe lower two layers of the earth’s atmos-phere: the troposphere and stratosphere.Ozone present in the troposphere is nor-mally found at concentrations of 10 to 30parts per billion. Tropospheric ozone hasincreased in recent decades in the NorthernHemisphere due to photochemical produc-tion from anthropogenic precursors (77).Over 90% of the earth’s ozone is present inthe stratosphere, which contains ozoneconcentrations of 10,000 parts per billion(77). The stratosphere extends from 16 to160 km (10 to 100 miles) above the earth’ssurface. The ozone layer refers to the re-gion of the stratosphere where ozone con-centrations are greatest, about 25 km abovethe earth’s surface. Stratospheric ozoneprovides a protective layer for the earth’ssurface and is essential for life on thisplanet. Ozone is known to play a key func-tion in moderating the climate of the earthby absorbing ultraviolet radiation from the

sun (UV-B) and essentially acts as a sun-screen for the planet (57). There is a strongcorrelation between decreased strato-spheric ozone and increased UV-B at theearth’s surface (77). Increases in sunburn,skin cancer, eye damage, crop damage, andother negative environmental impacts canresult from increased UV-B. Absorption ofUV radiation by ozone in the earth’s strato-sphere also creates heat, which moderatesthe earth’s temperature (57,77).

The episodic loss of ozone each springover the Antarctic continent was demon-strated by Farman et al. (19). The low tem-peratures that occur between midwinterand spring make the Antarctic stratospheresensitive to growth of inorganic chlorine,which depletes ozone (3,19,41). Mappingof the recurring and worsening ozone de-pletion event has been monitored withsatellite data each year since 1985 (Fig.1B) (45). Within 4 years, ozone loss in aregion the size of the Antarctic continentoccurred, and 70% of the total ozone col-umn content was lost during Septemberand October 1989 (64). The size of theozone “hole” varies from year to year, butincreases in the size of the hole over timehave occurred (64). The ozone holes of1992 and 1993 were the most severe onrecord (24,77). In 1995, the ozone layerhole over Antarctica was twice the size ofthe previous year and lasted three and ahalf months longer than previous recordsof depletion (45). Springtime depletion ofstratospheric ozone was recorded over theNorthern Hemisphere in the Arctic inMarch 1996 (45). Ozone levels were 20 to25% lower over Siberia, Europe, and partsof Canada than previous recorded levels(45).

Dr. Ristaino’s address is: Department of PlantPathology, North Carolina State University, Ra-leigh 27695-7616;E-mail: jean_ristaino@ ncsu.edu

Publication no. D-1997-0725-01F© 1997 The American Phytopathological Society

-

Plant Disease / September 1997 965

Atmospheric pollutants such as chloro-fluorocarbons and bromine react chemi-cally with ozone molecules (41). Halogen-ated hydrocarbons have been used aspropellants and refrigerants, and they in-clude compounds such as chlorofluorocar-bons (CFCs), hydrochlorofluorocarbons(HCFCs), the Halons, methyl chloroform,and carbon tetrachloride (77). These com-pounds remain in the atmosphere for 40 to150 years (41). Chlorofluorocarbons un-dergo photolysis in the stratosphere andproduce significant amounts of chlorine(77). Chlorine reacts with ozone andbreaks down the molecule. Bromine reactsin a similar manner to chlorine and is alsoa potent ozone depletor (3,77). At leastseven organic bromine compounds havebeen identified in the atmosphere (51).Bromoform, emitted from ocean sources,is a large contributor to atmosphericbromine and has a short lifetime due tophotolysis. Methyl bromide is the majorcarrier of bromine to the stratosphere (51).Methyl bromide breaks down to formbromine, which participates in a series ofozone-depleting chemical reactions(15,67). In fact, bromine is 50 times morereactive than chlorine in depleting ozonebecause it reacts with reservoir chlorinespecies, freeing the chlorine to react withadditional ozone (77).

A recent analysis by Montzka et al. ofair samples from around the world takenbetween 1991 and 1996 revealed that tro-pospheric chlorine attributable to anthro-pogenic halocarbons peaked near the be-ginning of 1994 and was decreasing at arate of 25 ppt per year by mid-1995 (42).Bromine from Halons is still increasing,but the summed abundance of the halogensis decreasing. The amount of reactive chlo-rine and bromine will reach a maximum inthe stratosphere between 1997 and 1999 ifall limits outlined in the Montreal Protocolon Substances that Deplete the OzoneLayer are not exceeded in future years(42). These results indicate that the regu-latory actions on a worldwide basis havemade an impact on levels of CFCs in thestratosphere (42). However, most of theCFCs measured in the work of Montzka etal. are still on the increase in the strato-sphere. The study did not include methylbromide in the analysis (42).

The Role of Methyl Bromidein Ozone Depletion

Unlike chlorine, which is present in thestratosphere mostly from human activities,presence of bromine compounds in theatmosphere can result from both naturaland anthropogenic sources (77). Four ma-jor atmospheric sources of methyl bromidehave been identified, including oceansources, which are a natural source, andthree anthropogenic sources, includingagriculture, biomass burning from destruc-tion of forests, and automobile exhaust

(13). Emissions of bromine from thesesources into the atmosphere have beenmeasured. Emissions of methyl bromidefrom natural ocean sources range from 26to 100 Gg per year (77). The largest an-thropogenic source of methyl bromide inthe atmosphere is agricultural use. Esti-mates of sources of methyl bromide fromsoil fumigation range from 16 to 47.3 Ggper year. Biomass burning emits 10 to 50Gg per year of methyl bromide. Emissionsfrom the exhaust of cars using leadedgasoline range from 0.5 to 22 Gg per year(77). Penkett et al. measured concentra-tions of methyl bromide in the atmosphereand found concentrations were higher inthe Northern than in the Southern Hemi-

sphere. These authors suggested that themajor source of emissions of methyl bro-mide entering the atmosphere was anthro-pogenic (51).

Research to determine the relative mag-nitudes of natural and anthropogenicsources of methyl bromide has led to muchdebate, and uncertainties still exist. Earlywork suggested oceans were a large netsource of methyl bromide (59), but recentwork suggests that oceans are a small netsink for methyl bromide (32). Annual oce-anic sinks for methyl bromide of 142 Ggper year were estimated (32). Most of themethyl bromide produced in the oceans (60to 75%) is degraded in situ in seawater bynucleophilic substitution by Cl- and by

B

Fig. 1. Methyl bromide and ozone depletion. (A) Commercial fumigation of agriculturalsoils with methyl bromide. (B) History of the Antarctic ozone hole from 1970 to 1993.

A


hydrolysis (2,18). The relative amount ofmethyl bromide emitted to the atmospherefrom ocean sources is still a subject ofgreat debate, and estimates from 30 to 90%of total production have been proposed(1,32). The magnitude of the flux ofmethyl bromide into and out of oceans isimportant since it affects the atmosphericlifetime of the compound and hence theozone depleting potential (ODP) (2). Only8% of the observed interhemispheric dif-ferences in methyl bromide concentrationswere attributed to oceanic sources andsinks (32). Current data indicate the im-portance of the oceans in buffering atmos-pheric bromine concentrations but alsoemphasize that anthropogenic sources ofmethyl bromide are significant. Furtherresearch is needed on the atmosphericchemistry of methyl bromide and its role inozone depletion (67).

Is Methyl Bromidefrom Soil Fumigation Releasedinto the Atmosphere?

The general consensus is that substantialretention and degradation of methyl bro-mide within agricultural soils is unlikely,and most is released into the atmospherefollowing soil fumigation (23,79,83). Inone study, 87% of the applied methyl bro-mide was emitted within 7 days aftercommercial fumigation and plastic re-moval at 95 h (79). Fumigated fields cov-ered with plastic film released 40% of theapplied methyl bromide (79). However,these measurements may be erroneouslyhigh due to errors in measurement of themass balance of the compound and lack ofcorrection for temperature effects on vola-tilization of the compound (83). In a recentstudy, after commercial fumigation in an

inland valley soil in California, 36% of themethyl bromide was released within 24 hand 63% was released after 18 days(82,83). Addition of irrigation during thefumigation process increased degradationof methyl bromide and reduced emissionsto 5%, presumably through hydrolysis ofthe compound (83). Other managementpractices, including deep injection of thefumigant and addition of organic matter tothe soil prior to fumigation, are being in-vestigated and may substantially reduceemissions of the fumigant to the atmos-phere. However, the addition of organicmatter may reduce the biocidal propertiesof the fumigant to soilborne pathogens andpests (44). Increased soil moisture willdecrease soil temperatures and could alsoreduce the effectiveness of the fumigant(44). New plastic films, termed virtuallyimpermeable films (VIF), have been de-veloped and tested in Israel, but controlledfield measurements of the mass balance ofmethyl bromide emitted after fumigationunder VIF tarps need to be conducted inthe United States. Bromine can accumulatein the groundwater and can be taken up byplants (27). Further experiments on reduc-tions in emissions of the fumigant areneeded, with particular emphasis on im-pacts of new tarping technologies on emis-sions, improvements in application tech-nology to reduce atmospheric releases, andeffects of these new technologies on plantpathogens and crop growth.

Some argue that most of the methylbromide applied during soil fumigation isdegraded or absorbed in soil and that thesoil is a large sink for methyl bromide (58).Bacterially mediated uptake of methylbromide in soils has been reported (58).Methyl bromide can undergo a variety ofreversible or irreversible processes in the

soil (8). In one study, chemical bondingand decomposition by hydrolysis had littleeffect on the flow of methyl bromidethrough soil columns (8). Degradation ofmethyl bromide and subsequent productionof bromine is highly dependent on soilorganic matter, with the greatest bromineproduction in muck soils and the least pro-duction in sand (5,8). Hydrolysis andmethylation are the two most commonmeans of degradation of methyl bromide insoils (11,32,38). Degradation of methylbromide in soil decreases with soil depth,mainly due to reduced organic matter (23).In soils with high organic matter, degrada-tion of methyl bromide by methylationpredominates over hydrolysis (23). Methylbromide can also undergo degradation inanaerobic sediments by bacterial metabo-lism from methanogenic and sulfate-re-ducing bacteria (49). The resulting methy-lated sulfur compounds serve as substratesfor methanogens and other bacteria presentin microbial films in salt marsh communi-ties. Coastal salt marshes containing sul-fate-reducing bacteria may constitute asink for atmospheric methyl bromide, butthe size of this sink is not clear at the pres-ent time (49).

Regulatory ActionConcern over ozone depletion led to ne-

gotiations among countries that resulted inthe 1987 drafting of the Montreal Protocolon Substances that Deplete the OzoneLayer (26,67). This ambitious environ-mental treaty set the standards for reduc-tions of ozone-depleting substancesworldwide and was signed by more than150 countries, including the United States.The treaty governs the production andtrade of ozone-depleting substances andrequires eventual elimination of productionof those substances. The Copenhagenamendments to the Protocol called for aban on all CFCs by 1996. An ozone deple-tion potential (ODP) index is used underthe Montreal Protocol and the Clean AirAct to gauge a substance’s relative poten-tial to deplete stratospheric ozone. TheODP represents the amount of ozone de-stroyed by the emission of 1 kg of a chosengas over a particular time scale comparedwith chlorofluorocarbon-11 (CFC-11), amajor ozone depletor (67). The UnitedNations Environment Programme (UNEP)calculated that methyl bromide had anODP of 0.6, or 60% of CFC-11’s ozone-depleting potential, and the atmosphericlifetime was calculated at 1.7 years(39,61). The ODP of methyl bromide isdependent upon the atmospheric abun-dance of chlorine. The higher theabundance of chlorine, the higher the ODPof methyl bromide. The relative value ofthe ODP of methyl bromide is importantsince gases with ODP greater than 0.2 arelisted as Class I ozone depletors and arerequired to be phased out under the U.S.

Table 1. Schedule of methyl bromide phaseout in the United States and in the internationalcommunitya

Provision United States Montreal Protocol

Freeze on productionand importation

Production and importationfrozen at 1991 levels,effective 1 January 1994

Production and importationfrozen at 1991 levels, effective1 January 1995

Exemptions to thefreeze

No exemptions have beengranted yet. EPA hasauthority to grant exemptionsfor use in medical devices andfor export to developingcountries.

Preshipment and quarantine usesexempted. Methyl bromideproduction can exceed their1991 levels by 10% to export todeveloping countries.

Ban on productionand importation

A ban on production andimportation becomes effectiveJanuary 2001.

Developed countries agreed tophase out use by 2010 with50% reduction by 2005, 25%reduction by 2001.

Developing countries agreed tofreeze use of methyl bromide in2002 based on averageproduction levels in 1995 to1998.

a From U.S. Government Accounting Office. 1995. Pesticides: The Phaseout of MethylBromide in the United States. GAO/RCED-96-16, Washington, DC.


Clean Air Act and the Montreal Protocol(67,71).

In December 1993, the EPA issued a no-tice of final rulemaking that added methylbromide to its list of Class I substances andestablished a domestic schedule for elimi-nation of production of the compound(Table 1) (43,71). Domestic production ofmethyl bromide in the United States wascapped at 1991 levels as of 1 January 1994,and use of the compound is to be elimi-nated by 2001 (71). After this date, no newimportation or production of methyl bro-mide can occur in the United States.Stronger international efforts to controlmethyl bromide emissions have also beendeveloped (77). In December 1995, partiesto the Montreal Protocol met, and devel-oped countries agreed to eliminate produc-tion of methyl bromide by 2010, with a50% reduction by 2005 and a 25% reduc-tion by 2001. Developing countries, whichcurrently account for only 18% of theglobal consumption of methyl bromide,agreed to freeze their use of the compoundin 2002 based on the average levels of1995 to 1998 consumption (43) (Table 1).

Methyl bromide is categorized as a re-stricted use pesticide, and registration iscurrently required under the Federal Insec-ticide, Fungicide, and Rodenticide Act(FIFRA). Methyl bromide is currentlyundergoing reregistration, and data sup-porting its registration are being suppliedby producers. The compound has acutetoxicity risks and requires special handlingby trained individuals to ensure safe use (53).

Methyl Bromide Sales and UseSince the Montreal Protocol

Sales. Methyl bromide production in theUnited States increased from 1984 to 1991and declined thereafter (Fig. 2A) (71). TheU.S. schedule for phaseout of methyl bro-mide called for a freeze on production ofmethyl bromide at 1991 levels effectiveJanuary 1994. The EPA’s StratosphericProtection Division in the Office of Airand Radiation is currently tracking theproduction, import, and export of methylbromide and calculating consumption rateseach year until 2001 (71). Consumption ofthe chemical is defined as annual produc-tion plus imports minus exports. U.S. ex-ports of methyl bromide declined from5,442 to 2,268 t between 1980 and 1984.Since 1984, U.S. exports of methyl bro-mide have nearly quadrupled and were 8,526t in 1995. The largest amount of methylbromide from the United States is exportedto western Europe, Canada, and Asia (68).

Annual worldwide production of methylbromide has increased over time (Fig. 2B).A worldwide summary of methyl bromidesales by region for 1984 to 1990 indicatesthat most of the sales of methyl bromideare in North America, Europe, and Asia(Fig. 3A). These regions account for 41.6,27.8, and 22.3% of the total sales of methyl

bromide (68). Mexico and Central Ameri-can and Caribbean countries are includedin the North American estimates of sales,but these countries are not large users ofmethyl bromide. The United States, Japan,and Italy are the top three user countries ofmethyl bromide (68). In North America,Europe, and Asia, sales of the product arepredominantly for preplant soil fumigation(Fig. 4A). Sales of methyl bromide forpreplant use as a soil fumigant have in-creased to a greater extent in North Amer-ica than in Europe, Asia, or other parts ofthe world (Fig. 4A) (68). In Asia, sales ofmethyl bromide from 1984 to 1990 forpostharvest treatment of exports to otherAsian countries greatly exceeded the post-harvest usage of methyl bromide for treat-ment in North America (Fig. 4B). In 1990,Asian sales were 5,265 t of methyl bro-

mide; whereas U.S. sales were only 1,219t. Most methyl bromide used in postharvestfumigation is released to the atmosphere.This indicates that Asian countries shouldbe targeted for recycling and alternativefumigant research and implementationefforts.

Use. Approximately 29,000 t of methylbromide were used in the United States in1990. More than 80% of the methyl bro-mide use in the United States is for agri-culturally related purposes. Most of the useof methyl bromide for preplant soil fumi-gation occurs on 21 small fruit and vegeta-ble crops in California, Florida, Georgia,North Carolina, and South Carolina (Fig.3B) (69). The largest uses of the fumigantby crop are for tomatoes, strawberries,peppers, ornamentals and nurseries, to-bacco, grapes, and melons. California and

Fig. 2. Methyl bromide production in (A) the United States from 1984 to1995 and (B)worldwide from 1984 to 1990.


Florida are the largest users of methylbromide in the United States, and most ofthe use is on strawberries and tomatoes,respectively (69).

Pesticide use data in California collectedby the California Department of PesticideRegulation are the most extensive in thecountry (10). An increase in methyl bro-mide use occurred from 1,451.2 t on 49commodities in 1971 to 8,707 t on 109commodities in 1992. Methyl bromide wasthe chemical alternative that replaced or-ganochlorines and other fumigants thatwere banned in the 1970s and 1980s. From1990 to 1994, field use of methyl bromideon strawberries in California declinedslightly, from 1,966 to 1,879 t, while hec-tarage of strawberries in California hasbeen stable between 9,430 and 9,470 ha(10). In recent years, use of methylbromide across all commodities inCalifornia declined slightly, from 9,100 to7,600 t, and number of applications alsodeclined between 1990 and 1994 (10,70).

Economic Impactof the Loss of Methyl Bromide

The National Pesticide Impact Assess-ment Program (NAPIAP) estimated annual

economic losses of $1.3 to 1.5 billion if aban of methyl bromide use occurred in theUnited States (69). Most of the losses es-timated were due to loss of soil fumigation($800 to 900 million), and lesser amountswere due to loss of quarantine fumigationfor imports ($450 million). NAPIAP esti-mates indicated that the greatest losseswould occur in tomatoes and strawberries.The USDA-NAPIAP study thoroughlyidentified regional areas of greatest use ofmethyl bromide and crops that had thegreatest dependence on the compound (69).The California Department of PesticideRegulation also conducted an economicanalysis of the loss of methyl bromide anddetermined that $287 to 346 million inlosses would result from the loss of the soilfumigant, and $241 million in trade incomewould be lost (9). In Florida, a ban ofmethyl bromide would affect tomatoes,peppers, cucumbers, squash, eggplant,watermelon, and strawberries. Estimatedlosses of more than $500 million wereprojected (62). These loss estimates as-sumed that few or no alternatives would beavailable or used.

The EPA conducted a cost–benefitanalysis of the elimination of methyl bro-

mide (unpublished data). The EPA esti-mated that $1.2 to 2.3 billion in lossescould occur if the methyl bromide phaseoutdid not occur. Additionally, EPA estimatedthe likely health effect costs of the use ofmethyl bromide. It was estimated that be-tween $244 and 952 billion in benefitswould result primarily from a reduction in2,800 skin cancer deaths over the periodfrom 1994 to 2010. Estimates of ozonedepletion and skin cancer incidence associ-ated with a “no restrictions” scenario, theless restrictive Montreal Protocol, and themost restrictive Copenhagen Amendmentshave been conducted (60). The no restric-tions and Montreal Protocol scenarios pro-duce runaway increase in the incidence ofskin cancers, up to quadrupling and dou-bling, by 2010, respectively. The Copenha-gen Amendments scenario leads to anozone minimum around the year 2000 anda peak relative increase in incidence ofskin cancer of almost 10% 60 years later.These results demonstrate the importanceof international measures agreed to underthe Vienna Convention to phase out ozone-depleting compounds (60).

Estimates on a global scale of the eco-nomic costs of reduced ozone need to becalculated as more scientific research isconducted to define the impacts of ozonedepletion on specific terrestrial and atmos-pheric ecosystems. These indirect costsneed to be examined so that balanced,sound policy on pesticide use can be de-veloped (52). Indirect costs of methyl bro-mide use include detrimental human healtheffects from increased UV-B (60), detri-mental effects of increased UV-B on globalphotosynthetic rates (57), health effectsfrom exposure of workers to the compound(53), increased control expenses resultingfrom pesticide-related destruction of bene-ficial organisms (40), yield reductions dueto phytotoxicity (40), groundwater con-tamination (7), and governmental expen-ditures to reduce the environmental andsocietal costs of the use of the pesticide,including alternative research and devel-opment in the United States and develop-ing countries.

Some workers have proposed that thephaseout of methyl bromide should bebased on the value of the use of the com-pound on specific commodities (80). Theeconomic effect of the elimination ofmethyl bromide varies by region and cropin California. Strawberries have the highestnet return per pound of methyl bromideused, so workers have suggested thatelimination of the compound should not beuniform on all crops but staggered bycommodity from low- to high-value usageto reflect these net returns (80). Addition-ally, a tax on usage of the fumigant hasbeen proposed that would result in a priceincrease and thus reduce usage of the fu-migant over time from 8,617 to 2,494 t inCalifornia (80). Pesticide use fees havebeen proposed by others as an alternative

Fig. 3. Methyl bromide (A) total sales (% metric tons) by region of the world from 1984to 1990 and (B) consumption by end use in 1990.


to outright banning of specific pesticides.Such fees could be used to support IPMresearch and environmental regulatoryactivity but might not reduce the actualusage of compounds (50,87). However,risk-adjusted taxes, with higher use fees forcompounds with more serious environ-mental impact, create incentives for usersto choose less hazardous and less expen-sive products, according to Pease et al.(50). Taxation of methyl bromide wouldrequire new national legislation (43). With-out alternatives, outright pesticide bansresult in reduced production levels, higherprices for consumers, and possible use ofmore toxic compounds by growers (87).

Trade Issues Relevantto Phaseout of Methyl Bromide

U.S. law requires that certain agricul-tural imports from specified countries bealmost completely (99.9968%) pest freeprior to entry (69). Methyl bromide fumi-gation is one of the quarantine treatmentsaccepted by USDA, and it is often the pre-ferred method of treatment at ports of entryinto the United States. Many importedfruits and vegetables enter the UnitedStates during months when similar com-modities are unavailable locally. In addi-tion, more than $400 million worth ofexports were fumigated with methyl bro-mide in 1994 (72). Over 118 millionkilograms of cargo was fumigated for im-port or export in California alone in 1996(9). Methyl bromide is the fumigant ofchoice for quarantine purposes since itrequires short treatment times, is effica-cious, has a low cost, and does not affectquality or flavor of the treated commodityif used correctly (9). The total use ofmethyl bromide for quarantine treatmentsin the United States is less than 1% of itsuse for preplant soil fumigation (Fig. 3B).Whether exemptions will be granted forcertain restricted uses of methyl bromidesuch as quarantine has not yet been deter-mined (72).

If methyl bromide use is banned in theUnited States as a quarantine treatment,alternative methods of treating import andexport commodities will be needed. Alter-native treatments are currently being usedby USDA Animal Plant Health InspectionService (APHIS) to treat commodities, andmany USDA and university laboratoriesare working on this issue (Table 2). Thepros and cons of the use of alternative fu-migants for stored products have beenreviewed (65,68,81). Several quick, effi-cient technologies, including microwavesand irradiation, may prove useful as alter-natives for quarantine treatment of storedproduct pests (20). Movement of pests andpathogens across borders could increase ifalternative strategies for quarantine fumi-gation are less effective than methyl bro-mide. APHIS is increasing emphasis onpest risk assessment to more precisely

estimate risks and reduce the number ofphytosanitary applications of fumigants.Tolerance levels for certain pests based onrisk need to be developed. Increased use ofaccurate diagnosis and deployment of mo-lecular detection methods for pests andpathogens into quarantine decision makingcould significantly reduce the use of fumi-gation.

The proposed international phaseout ofmethyl bromide differs from the domesticschedule for phaseout (Table 1). This hasled U.S. growers to be concerned that anunfair trade advantage may be gained byother nations if U.S. growers are forced toeliminate methyl bromide use by 2001. Inparticular, Florida tomato growers are con-cerned that Mexican growers may developan even greater competitive edge in fresh-market tomatoes if Florida can no longerfumigate its fields with methyl bromide

(62). Over 95% of the tomato fields inFlorida are currently fumigated withmethyl bromide due to problems fromsoilborne diseases including the root-knotnematode, Fusarium, and bacterial wiltdiseases (70). Over 95% of the Mexicanfresh-market tomato growers do not cur-rently use methyl bromide since soilbornepathogens are less severe in their tomato-growing areas. Methyl bromide use inMexico is primarily for strawberries grownin the Baja region (34). Despite their use ofthe fumigant, Florida shipments of toma-toes account for 45.2% of the market,while Mexican exports have increaseddramatically in the United States in the lastyear and now account for 40.7% of themarket (73). Apparently, issues other thanmethyl bromide use, including reducedlabor costs, improved varieties and pro-duction practices in Mexico, and consumer

Fig. 4. Methyl bromide sales by region of the world for (A) preplant soil fumigationand (B) postharvest fumigation, from 1984 to 1990.


choice of Mexican tomatoes that are vineripened rather than gassed, have influencedthis increase in Mexican imports (34,73).

Alternatives to Methyl BromideAlternative fumigants. The pending

elimination of methyl bromide use in the

United States has stimulated a great deal ofcreative research that should improve ourability to manage soilborne pathogens us-ing ecologically based pest managementstrategies. It is clear from most of the re-search conducted to date that a single al-ternative fumigant will not be found to

replace methyl bromide, although recently,workers have suggested that methyl iodidemight be that new alternative (47). Somewould argue that it is not desirable that asingle new “magic bullet” fumigant befound that is as efficacious and widelyapplicable as methyl bromide. Use of adiversity of management practices thatinclude less dependence on single-chemi-cal strategies and greater use of biologicaland cultural management strategies couldenhance grower options (46). On the otherhand, if a single chemical method of con-trol that is safe and efficacious could befound to replace methyl bromide, it wouldbe rapidly adopted by growers (53).

Methyl iodide has shown promise as auseful soil fumigant and has not been im-plicated as an ozone depletor (47) (Table3). Methyl iodide has an atmospheric life-time of 1 week in the troposphere and israpidly oxidized. Methyl iodide was equalto or better than methyl bromide in con-trolling Phytophthora citricola, P. cinna-momi, P. parasitica, Rhizoctonia solani;the nematode Heterodera schachtii; andthe weed plants Cyperus rotundus, Poaannua, Portulaca oleracea, and Sisym-brium irio (47). The compound is not cur-rently registered, although EPA has re-ceived some inquiries from prospectiveregistrants about the compound.

Strawberries are susceptible to a numberof soilborne and fruit-rotting pathogens,including Rhizoctonia solani (Fig. 5A),Phytophthora fragariae (Fig. 5B), P. citri-cola, P. cactorum, root-knot nematodesMeloidogyne incognita and M. hapla (Fig.5C), Verticillium dahliae, and black rootrot caused by a complex of Pratylenchus

Table 3. Chemical alternatives to methyl bromide

Chemicalname

Crop Pest or pathogen Comments

Chloropicrin Strawberries, fruit and nut crops,Solanaceous, leafy vegetables,forestry and nursery crops

Nematodes, soil insects, soilfungi (Fusarium, Pythium,Rhizoctonia, Sclerotinia,Verticillium, and Colletotrichum)

Drift problems. Marginal activity against somenematodes and weeds due to poor distribution in soil.Reregistration early 1997.

Dazomet(Basamid)

Solanaceous (tobacco seedbed only),forestry, ornamental and nurserycrops

Nematodes, soil insects, soilfungi, and weed seeds

Long period between application and planting. Highlyphytotoxic. Registered for nonfood crops use currently.Experimental use permit granted on strawberries,peppers, tomatoes, and broccoli in February 1996.Registration decision, early 1998.

1,3,Dichloro-propene(Telone II)

Vegetables, tobacco, and root cropsmostly, but labeled for all food andnonfood crops

Nematodes, soil insects, soilfungi

In special review because of cancer concerns. Labelchanges to mitigate risk agreed to by registrant.Restricted usage in California due to residue problemsin air samples around urban areas adjacent to farmland.Special review by EPA will be done in 1997.

Telone C-17 Vegetables, tobacco, and root cropsmostly, but labeled for all food andnonfood crops

Nematodes, soil insects, soilfungi

Same as Telone II but with added chloropicrin. Sameconcerns as above.

Methyliodide

Not labeled yet for any crop Soil fungi, nematodes, weeds Not registered currently. Destroyed rapidly introposphere. One week atmospheric lifetime.

Metam-sodium(Vapam)

Strawberries, fruit and nut crops,leafy vegetables, forestry, nurseryand ornamental crops

Nematodes, weeds, soil fungi,insects

Reregistration scheduled for early 1998. Major spill inSacramento River caused environmental problems. Notas efficacious as Telone on strawberries. Can be usefulat low rates with biological control agents.

Table 2. Postharvest pest control strategies and potential alternativesa for methyl bromide

Treatment Treatmenttime

Comments and issues

Methyl bromide 3 to 12 h Ozone depletion, 2001 phaseout. Quickefficacious treatment.

Methyl bromidewith recapture

3 to 12 h Scale up to large-scale recapture difficult, efficacy.

Phosphine 4 to 7 days Registered. Resistance development, longer timefor treatment. Least disruptive to currentpractices.

Controlledatmosphere (C02)

3 to 40 days Slow acting and temperature dependent. May helpripen and disinfect. Storage facilities needupgrading.

Cold 3 to 40 days Slow acting and energy intensive. Extends productshelf life. Relatively safe.

Dust anddiatomacaeousearth

Days to weeks Inert dust sprayed in empty storage bins andequipment. Crawling insects are desiccated.

Heat 1 to 36 days Energy intensive. Can affect quality. Vapor, hotwater, dry heat.

Microwave <1 h Microwave energy applied as grain enters bin.Cost comparable to chemical treatment.

Irradiation <1 h Consumer reluctance. Short treatment time of <1h. Extends shelf life. Expensive process.

Biological Agent specific Nontoxic, long-term solution. Control but noteradication. Quarantine issues.

Certified pest-freezone

No treatmentrequired

Requires extensive monitoring, may increasepesticide use. Product shelf life and qualityunaffected.

a List of alternatives from references 65, 68, and 81.


penetrans and Rhizoctonia and Pythiumspecies (Fig. 5D) (86). Strawberry produc-ers in California are among the largestpreharvest users of methyl bromide. Anumber of soil fumigants are available thatcould provide alternatives to methyl bro-mide use in specific applications forspecific pests or pathogens (Table 3)(4,6,17,31). Field experiments were con-ducted in commercial fields with five pre-plant treatments, including methyl bro-mide/chloropicrin (67/33% at 364 kg/ha),chloropicrin (336.3 kg/ha), Telone II(1,3,dichloropropene)/chloropicrin (70/30%at 509 kg/ha), Vapam (metam-sodium,993.58 liters/ha), or no treatment (17).Fumigants were broadcast treated undertarpaulins, and after 5 days covers wereremoved, beds were shaped, and straw-berries were planted. In a second test,Vapam was replaced with Telone II(1,3,dichloropropene)/chloropicrin (30/70%at 458 kg/ha). All fumigants tested, withthe exception of Vapam, worked equallywell, and yields were not different from themethyl bromide–treated plots in 1994 and1995, when the fumigants were used athigh rates in soil with a history ofstrawberry/vegetable rotations (17).Disease pressure was low in the fieldstested, and growth responses were ob-served in the absence of disease (17). In1996, in fields where disease pressure washigher, yields were increased over the non-fumigated controls in all fumigant treat-ments; however, yields were highest withthe methyl bromide/chloropicrin mixture(17). These studies on strawberries arecurrently in progress in California, andabstracts of the work have been published(17). The rates of alternative fumigants andcosts are economically feasible for straw-berry growers (66). Telone use in Califor-nia is currently restricted by the CaliforniaDepartment of Pesticide Regulation due totoxicity and excessive residues in air sam-ples collected from treated fields nearschools (7). Permit conditions allow use of18,927 liters for shallow injections or35,961 liters for broadcast or deep injec-tions per township range (93 km2) per year.Telone II is also currently under specialreview at EPA. Clearly, some cost-effec-tive alternative soil fumigants will beavailable by the 2001 phaseout date (Table3) (66). The best long-term solution forstrawberry producers will be the develop-ment of resistant varieties, crop rotations,planting of pathogen-free planting materi-als, and judicious use of low-riskpesticides (17,25,31,66). Use of moleculardetection methods for certification ofpathogen-free planting materials could alsoreduce introduction of strawberrypathogens such as Verticillium andPhytophthora species into fumigated soils.

Resistant varieties. Host resistance isone potential long-term solution for man-agement of the major soilborne pathogensof both strawberry and tomato. Currently,

few strawberry varieties grown commer-cially in California have resistance to themajor strawberry pathogens, includingPhytophthora species and V. dahliae(31,75). Research has been conducted inother areas of the United States and is inprogress in California to develop host re-sistance to root-infecting fungi onstrawberry (35,75). Most of the breedingefforts in California have focused on de-velopment of high-yielding varieties withgood shipping qualities and other desirableagronomic traits (31). Currently grownstrawberry cultivars have greater differ-ences in levels of resistance to Phy-tophthora species than to Verticillium spe-cies, but these levels of resistance are notequal to the beneficial effects observedwith soil fumigation (75). Further researchis needed to develop resistant strawberrycultivars adaptable to growing conditionsin California and elsewhere.

Many tomato varieties have resistance toFusarium oxysporum, nematodes, and V.dahliae. The challenge is to maintain levelsof resistance to these pathogens as newraces occur in the field. Some novel ap-proaches using transgenic gene technolo-gies have been developed that may providemore specific resistance to root-infectingnematodes (48). Specific plant genes canbe turned on at nematode feeding sites inorder to stop giant cell formation in roots

(48). Continued research utilizing bothtraditional and molecular strategies will beneeded to develop host resistance to anumber of soilborne pathogens to accept-able levels for many vegetable crops.

Biological alternatives and culturalpractices. Soil quality is the capacity ofsoil to function, within ecosystems andland-use boundaries, to sustain biologicalproductivity, maintain environmental qual-ity, and promote plant, animal, and humanhealth (16). Mycorrhizal fungi are detri-mentally impacted by methyl bromidefumigation in soils from diverse croppingsystems (40). Microbial biomass in fumi-gated forest and pasture soils consistentlyremains lower than in nonfumigated soilseven after 6 months (85). Bacteria are lessaffected by soil fumigation and recovermore rapidly than do fungi in fumigatedstrawberry field soils (17,85). Diversity ofprotozoans and nematodes is greatly re-duced by the fumigation process (85).Beneficial nematodes including bac-terivores, fungivores, omnivores, andpredators are major components of thebiological soil food web and also playimportant roles in nutrient cycling in soils(84). In fact, these nematodes can providea useful indicator of soil health, and theirelimination from fumigated soil could leadto negative long-term consequences forsoil productivity (84).

Fig. 5. Strawberry pathogens, including(A) Rhizoctonia solani on fruit, (B) redstele caused by Phytophthora fragariaeshowing infected plant and internal viewof red stele, and (C) northern root-knotnematode Meloidogyne hapla in strawberryroot tissue. (D) Black root rot causedby a complex of pathogens, includingPratylenchus penetrans, Rhizoctonia spe-cies, and Pythium species.

A C

B

D


Fumigated soils can also provide openniches for recolonization by pathogenicfungi (37). Introduced pathogens spreadrapidly in fumigated soils that are devoidof suppressive biological communities(37). In a typical raised-bed fumigation,soil in furrows is not fumigated and canprovide an inoculum source for introduc-tion of pathogens into fumigated soils.Fusarium species rapidly colonize fumi-gated soils and can spread to cause severedisease in the absence of competition frombeneficial microorganisms (37). Simplechanges in cultural practices, such as theplanting of pepper in stubble from a no-tillcover crop of wheat or rye-vetch, can sub-stantially suppress the dispersal of Phy-tophthora capsici in fumigated soil (54).

Solarization involves the thermal heat-ing of moistened soil by sunlight underclear plastic mulch to temperatures that arelethal to a broad spectrum of soilbornepathogens, insects, and weeds (29). Solari-zation is generally conducted for 3 to 6weeks in the hottest part of the year (29).Beneficial microorganisms such as ther-mophilic organisms and some bacteriasurvive solarization and act as antagonistsagainst weakened plant pathogens (55). Incontainerized soil, solarization may beconducted within 1 week under Californiaconditions (63). Soil solarization is a po-tential alternative practice for control ofsoilborne pathogens in southern coastalCalifornia, Florida, Texas, and NorthCarolina (12,28,55). Solarization has beenused on a wide variety of crops and is ef-

fective against a number of important soil-borne pathogens, including Sclerotiumrolfsii (Fig. 6A), V. dahliae, and Phy-tophthora species (29,52). In North Caro-lina, repeated field tests have demonstratedthe efficacy of soil solarization for controlof southern blight caused by S. rolfsii onbell pepper, carrot, and tomato (55,56).

Solarization was as effective as methylbromide in reducing baited populations ofP. cactorum and P. citricola in strawberryfield soils, but reductions in V. dahliaepopulations were not as large (28). Yieldswere similar between methyl bromide–treated plots and solarized plots, but higherwith the fumigant treatment (28). Straw-berries are grown as an annual crop inmany areas of the United States, and fieldshave a summer fallow period that is idealfor solarization. Solarization would proba-bly not be as reliable as chemical fumiga-tion for coastal strawberry production areasin California since regional variations insolar radiation occur in coastal areas. So-larization experiments are needed on awider scale in marginal areas to confirm orrefute this idea. In the San Joaquin Valley,where temperatures are higher, solarizationmight be a viable alternative; but currentlymost strawberry acreage in California is incoastal areas (6). Soil temperature model-ing studies are currently being conductedon a regional basis in California with amodel developed at North Carolina StateUniversity (78). This work may potentiallyincrease the use of solarization as a pestcontrol strategy in California and else-

where (James Stapleton, University ofCalifornia, Davis, personal communica-tion).

Florida uses more methyl bromide intomato production than any other state forcontrol of a number of soilborne patho-gens, including Fusarium oxysporum f. sp.solani (Fig. 6B), Pseudomonas solana-cearum (Fig. 6C), root-knot nematodes(Fig. 6D), nutsedge, and other weeds (69).In 1994, soil solarization was comparedwith methyl bromide/chloropicrin for con-trol of soilborne pathogens of tomato (12).Soil solarization significantly reduced den-sities of Phytophthora nicotianae andPseudomonas solanacearum down todepths of 25 and 15 cm, respectively (12).However, Fusarium oxysporum f. sp. ly-copersici and F. oxysporum f. sp. radicis-lycopersici were reduced only in the upper5 cm of soil by solarization (12). Thisposes a problem since the Fusarium spe-cies can rapidly recolonize soils. In con-trast, fumigation with methyl bromidereduced levels of the pathogens to 35 cm(12). Incorporation of biological controlorganisms into solarized soils after solari-zation may improve control of Fusariumdiseases (30). Specific nonpathogenic iso-lates of F. oxysporum consistently reduceddisease by 50 to 80% when transplantmixes were treated with the antagonists.These isolates are currently being fieldtested in Florida in fields with a history ofFusarium wilt (R. Larkin, USDA,Beltsville, MD, personal communication).

Solarization of compost-amended soilswas highly effective at reducing popula-tions of root-knot nematode on lettuce(22). Soils solarized after incorporation ofcabbage residues produced volatile com-pounds that effectively suppressed Pythiumultimum and S. rolfsii (22). Alcohols, alde-hydes, sulfides, and isothiocyanates wereproduced in heated soil containing cabbageresidues. The cabbage residues were driedand ground and amended to soil prior toheating.

Electrical heating can reduce the inci-dence of soilborne pathogens in nurserysoils. Steam has been traditionally used innursery production systems but does notkill Fusarium spores present deep in soils(36). Ohmic heating involves passing anelectrical current between an anode and acathode in the soil. Heat is generated dueto the soil’s resistance to the current flow.Steel rods are driven in soil and act as an-ode and cathode arrays. Preliminary ab-stracts from the research indicate that Oh-mic heating was more effective than steamtreatment for reduction of Fusarium sporespresent deep in soil (36). This technologyhas been used in greenhouse systems, butlarge-scale applications for field use needfurther research.

Organic amendments may provide an-other means of suppressing plant patho-gens and improving soil quality (31,74).Organic growers use manures and cover

Fig. 6. Disease caused by (A) Sclerotium rolfsii on carrots. Sclerotia and myceliumpresent at the base of the plant. (B) Fusarium wilt caused by Fusarium oxysporum f.sp. lycopersici on tomato. (C) Internal stem discoloration in tomato caused by thebacterial wilt pathogen Pseudomonas solanacearum. (D) Root-knot nematode causedby Meloidogyne incognita on tomato roots.

A

B

C

D


crops as sources of nutrients. Organicstrawberry production systems are eco-nomically viable since price premiums areobtained even though yields are not as highas in conventional fumigated fields (6,25).In a study of conventional and organictomato production systems in California,Phytophthora root rot on tomatoes waslowest in soils with highest organic mattercontent and highest soil microbial activity(74,76). Soils with a diversity of beneficialmicroorganisms are more suppressive topathogens and pests than are soils that havelittle or no biological diversity. In thecoastal plains region of North Carolina,large-scale swine production facilities arelocated adjacent to vegetable farms. Most

of these farms contain soil that has beendepleted of organic matter. We are cur-rently testing swine manures for suppres-sion of soilborne plant pathogens in tomatoproduction systems (J. Ristaino and L. R.Bulluck, unpublished).

Incorporation of biological control or-ganisms into solarized, fumigated, ornontreated soils also shows promise forcontrol of a number of soilborne pathogens(14). Alginate bran prill formulations ofGliocladium virens incorporated intonontreated or solarized soils effectivelycontrolled southern blight caused by S.rolfsii to depths of 30 cm in field soils inrepeated studies (55,56). Application of theantagonists Talaromyces flavus and Glio-

cladium roseum in combination with lowrates of fumigation with Vapam (metam-sodium) reduced the incidence of Verticil-lium wilt on eggplant (21).

There are currently 13 biopesticidesregistered by the Biopesticides and Pollu-tion Prevention Division of the EPA thatare targeted for soilborne or postharvestpathogens (Table 4). In 1995, 20 new bio-pesticides were registered by EPA, and theagency has placed low-risk pesticides onthe fast track for registration. SoilGard(formerly GlioGard) was the first fungalbiological control agent registered with theEPA. It contains chlamydospores of thefungus Gliocladium virens. This beneficialantagonist has activity against Pythium andRhizoctonia in greenhouse potting mixesand against S. rolfsii in the field (33).Worldwide, there are 40 biocontrol prod-ucts commercially available to controlplant diseases; however, many of these arenot currently registered in the UnitedStates (33). Many of these biocontrol or-ganisms have broad-spectrum activityagainst a wide range of pathogens. Forinstance, Trichoderma species control spe-cies of Armillaria, Botrytis, Chondro-stereum, Colletotrichum, Fulvia, Monilia,Nectria, Phytophthora, Plasmopara, Pseu-doperonospora, Pythium, Rhizoctonia,Rhizopus, Sclerotinia, Sclerotium, Verticil-lium, and wood rot fungi (33). Myrothe-cium verrucaria (DiTerra) is a new bio-logical nematicide with activity against anumber of important nematodes species(Table 4). Biological control organisms canbe used as part of an integrated pest man-agement program to target specific patho-gens and pests. Most of the biologicalcontrol organisms currently on the marketare targeted for soilborne and postharvestdiseases. Some of these organisms couldbe used as alternatives to methyl bromideto target problem areas in fields (33).

Future OutlookThe development of sustainable produc-

tion practices for strawberries, tomatoes,and other high-value fruit and vegetablecrops without reliance on methyl bromidewill require the input of knowledgeableand progressive growers, industry repre-sentatives, scientists, environmentalists,regulatory agencies, and policymakers. Allthese groups need to come to the bargain-ing table and consider the short-term andlong-term impacts of their actions on theenvironment. The courtroom and the con-ference room are currently being used toresolve issues surrounding the use ofmethyl bromide. The debate over methylbromide has often resulted in polarizedviews by environmentalists, industrygroups, grower groups, regulatory agen-cies, and scientists. Agricultural scientistshave an important role to play in providingrelevant data to policymakers.

A number of creative, ecologically based

Table 4. Biopesticides registered by the Division of Biopesticides at the EnvironmentalProtection Agency with efficacy against soilborne and postharvest pathogens

Microbe and trade name Pest and crop

Agrobacterium radiobacterGallTrol-A

Crown gall caused by A. tumefaciens on fruit,nut, and ornamental nursery stock.

Bacillus subtilis GBO3Kodiak - Gus 2000 Biological fungicide

Rhizoctonia solani, Fusarium spp., Alternariaspp., and Aspergillus spp. - seed treatment onall crop seed.

Bacillus subtilis MBI 600Epic - Gus 376 Concentrate BiologicalFungicide

Rhizoctonia solani, Fusarium spp., Alternariaspp., and Aspergillus spp. - seed treatment oncorn, cotton seed, pod vegetables, peanuts,soybean, wheat, and barley.

Candidia oleophila I-182Aspire

Botrytis spp. and Penicillium spp. on citrus andpome fruits.

Gliocladium virens GL-21SoilGard

Pythium and Rhizoctonia in greenhouse soillesspotting mixes and soils. Efficacy also againstSclerotium rolfsii in field but not currentlyregistered for this use.

Myrothecium verrucariaDiTerra

Nematodes including Meloidogyne spp.,Heterodera/Globodera (cyst), Pratylenchusspp. (Lesion), Tylenchulus semipenetrans(citrus), Trichodorus spp. (stubby-root),Xiphinema spp. (Dagger) and other tylenchidnematodes of all food, fiber, and ornamentalcrops.

Pseudomonas fluorescens EG-1053Dagger

Pythium and Rhizoctonia on cotton.

Pseudomonas fluorescens NCIB 12089Victus

Bacterial blotch of mushroom caused byPseudomonas tolaasii. Applied to compostbeds.

Burkholderia (Pseudomonas) cepacia typeWisconsin

Deny (formerly Blue Circle)SMP PcpWi

Rhizoctonia, Pythium, and Fusarium spp. andlesion, spiral, lance, and sting nematodes onalfalfa, beans, canola, carrot, clovers, colecrops, corn, cotton, grain, lettuce, melons,potatoes, squash, sugar beet, sunflower,sorghum, soybeans, and tomatoes.

Pseudomonas syringae ECC-10, ESC-11Bio-Save 10Bio-Save 11

Penicillium expansum, P. italicum, P. digitatum,Botrytis cinerea, Mucor piriformis, andGeotrichum candidum for use on apples,lemons, grapefruits, pears, and oranges tocontrol fruit rots during storage.

Streptomyces griseoviridis K61Mycostop

Fusarium, Alternaria, Botrytis, Phomopsis,Pythium, and Phytophthora spp. on field cropsincluding beans, cotton, peas, sorghum,soybeans, wheat, and on vegetables andornamental crops in the field and greenhouse.

Trichoderma harzianum T-22 (KRL-AG2)RootshieldBiotrek (formerly F-Stop BiologicalFungicide Concentrate and SeedProtectant)

Pythium, Rhizoctonia solani, Fusarium spp.,and Sclerotinia homoeocarpa on beans,cabbage, corn, cotton, cucumbers, greenhouseornamentals, peanuts, potatoes, sorghum,soybeans, sugar beets, tomatoes, and turf.


approaches to disease and pest manage-ment have emerged from the debate overmethyl bromide use that may not havebeen developed without the impending lossof this compound. The formation of theBiopesticides and Pollution PreventionDivision in November 1994 at the EPA andthe registration of 36 new biopesticidessince 1995 are positive signs. Industryincentives are needed to develop low-riskpesticides and biologically based pesti-cides. The USDA has mobilized researchresources to develop alternatives to methylbromide. Priority registration of low-riskpesticides and biopesticides has been initi-ated at the EPA. Grower incentives in-cluding special subsidies that encourageuse of low-risk pesticides and biologicallybased pest management strategies are alsoneeded. Could green grower awards thatutilize “moral persuasion” be enacted bypartnerships between the USDA and EPAto reward growers who make the move toalternative, low-risk strategies for diseaseand pest management?

Research funded by the USDA and EPAhas provided opportunities for develop-ment of feasible alternatives to methylbromide. Recently, the agencies havejointly sponsored a yearly Methyl BromideAlternatives and Emissions Reductionmeeting. Many published research projectsand abstracts from yet-to-be-published

work have been shared at these meetings.Viable alternatives and technologies thatlead to reduced emissions are on the hori-zon. Additional funding is needed to con-duct IPM demonstration projects on com-mercial grower farms. Industry,government, and university partnershipscould lead to technological successes thatany partner alone might not achieve. Theseapproaches could redirect conventionalagriculture toward more sustainable, envi-ronmentally friendly methods of food pro-duction that minimize global ecosystemimpact in the twenty-first century and be-yond (46).

AcknowledgmentsA portion of this report was prepared during the

senior author’s tenure as a Fellow under theAmerican Association for the Advancement ofScience/U.S. Environmental Protection AgencyFellowship Program during the summer of 1996.Mention of trade names of commercial productsdoes not constitute endorsement or recommenda-tion. For further information on the phaseout ofmethyl bromide and alternatives contact BillThomas at the EPA web site at http://www.epa.gov/ozone/mbr/mbrqa.html.

Literature Cited 1. Albritton, D. L., and Watson, R. T. 1992.

Methyl bromide and the ozone layer; a sum-mary of current understanding. Pages 3-18 in:Methyl bromide: Its Atmospheric Science,Technology, and Economics, Montreal Proto-

col Assessment Supplement. R. T. Watson, D.L. Albritton, S. O. Anderson, and S. Lee-Bapty, eds. United Nations Environment Pro-gramme, Nairobi, Kenya.

2. Anbar, A. D., and Yung, Y. L. 1996. Methylbromide: Ocean sources, ocean sinks, andclimate sensitivity. Global Biogeochem. Cy-cles 10:175-190.

3. Anderson, J. G., Brune, W. H., Lloyd, S. A.,Toohey, D. W., Sander, S. P., Starr, W. L.,Loewenstein, M., and Podolske, J. R. 1989.Kinetics of O3 destruction by ClO and BrOwithin Antarctic vortex-An analysis based onin situ ER2 data. J. Geophys. Res. 94:11,480-11,520.

4. Anis, P. C., and Waterford, C. J. 1996. Alter-natives-Chemicals. Pages 275-321 in: TheMethyl Bromide Issue. C. H. Bell, N. Price,and B. Chakrabarti, eds. John Wiley & Sons,New York.

5. Arvieu, J. C. 1983. Some physico-chemicalaspects of methyl bromide behavior in soil.Acta Hortic. 152:267-274.

6. Baker, B. 1993. California strawberries: Pes-ticides used and their alternatives. J. Pestic.Reform 13:24-28.

7. Braun, A. L., and Supkoff, D. M. 1994. Op-tions to methyl bromide for the control ofsoilborne diseases and pests in Californiawith reference to the Netherlands. CaliforniaEnvironmental Protection Agency, Depart-ment of Pesticide Regulation, Pest Manage-ment and Analysis Division, Publ. No. 94-02.

8. Brown, B. D., and Rolston, D. E. 1980.Transport and transformation of methyl bro-mide in soils. Soil Sci. 130:68-75.

9. California Department of Food and Agricul-ture. 1996. Methyl Bromide: An Impact As-sessment. Office of Pesticide Consultation

An advertisement appears in the printed journal in this space.


and Analysis, Sacramento, CA. 10. California Environmental Protection Agency.

1990-1994. Pesticide Use Reports, AnnualSummaries Indexed by Chemical 1990-94.Department of Pesticide Regulation, Sacra-mento, CA.

11. Castro, C. E., and Belser, N. O. 1981. Photo-hydrolysis of methyl bromide and chloropic-rin. J. Agric. Food Chem. 29:1005-1008.

12. Chellemi, D. O., Olson, S. M., and Mitchell,D. J. 1994. Effects of soil solarization andfumigation on survival of soilborne pathogensof tomato in northern Florida. Plant Dis.78:1167-1172.

13. Cicerone, R. J. 1994. Fires, atmosphericchemistry, and the ozone layer. Science263:1243-1244.

14. Cook, R. J., and Baker, K. F. 1983. The Na-ture and Practice of Biological Control ofPlant Pathogens. American PhytopathologicalSociety, St. Paul, MN.

15. Cox, R. A., Rattigan, O. V., and Jones, R. L.1995. Laboratory studies of BrO reactions ofinterest for the atmospheric ozone balance.Pages 47-64 in: The Chemistry of the Atmos-phere: Oxidants and Oxidation in the Earth’sAtmosphere. A. R. Bandy, ed. Royal Societyof Chemistry, Cambridge.

16. Doran, J. W., and Parkin, T. B. 1994. Definingand assessing soil quality. Pages 3-21 in: De-fining Soil Quality for a Sustainable Envi-ronment. J. W. Doran, D. C. Coleman, D. F.Bezdicek, and B. A. Stewart, eds. Soil Sci.Soc. Am. Spec. Pub. No. 35.

17. Duniway, J. M., and Gubler, D. 1996. Evalua-tion of some chemical and cultural alterna-tives to methyl bromide fumigation of soil ina California strawberry production system.

Pages 37-1 to 37-2 in: Proc. 1996 Annu. Int.Conf. Methyl Bromide Alternatives EmissionReductions.

18. Elliot, S., and Rowland, F. S. 1993. Nucleo-philic substitution rates and solubilities formethyl halides in seawater. Geophys. Res.Lett. 20:1043-1046.

19. Farman, J. C., Gardiner, B. G., and Shanklin,J. D. 1985. Large losses of total ozone in Ant-arctica reveal seasonal ClOx/NOx interaction.Science 315:207-210.

20. Forsythe, K. W., Jr., and Evanylou, P. 1994.Costs and benefits of irradiation versusmethyl bromide fumigation for disinfestationof U.S. fruit and vegetable imports. U.S. Dep.Agric. Econ. Res. Serv.

21. Fravel, D. R. 1996. Interaction of biocontrolfungi with sublethal rates of metham sodiumfor control of Verticillium dahliae. Crop Prot.15:115-119.

22. Gamliel, A., and Stapleton, J. J. 1993. Char-acterization of antifungal volatile compoundsevolved from solarized soil amended withcabbage residues. Phytopathology 83:899-905.

23. Gan, J., Yates, S. R., Anderson, M. A.,Spencer, W. F., Ernst, F. F., and Yates, M. V.1994. Effect of soil properties on degradationand sorption of methyl bromide in soil. Che-mosphere 29:2685-2700.

24. Gleason, J. F., Bhartia, P. K., Herman, J. R.,McPeters, R., Newman, P., Stolarski, R. S.,Flynn, L., Labow, G., Larko, D., Seftor, C.,Wellemeyer, C., Komhyr, W. D., Miller, A. J.,and Planet, W. 1993. Record low global ozonein 1992. Science 260:523-526.

25. Gliessman, S. R., Werner, M. R., Swezey, S.L., Caswell, E., Cochran, J., and Rosado-May,F. 1996. Conversion to organic strawberry

management changes ecological processes.Calif. Agric. 50:24-31.

26. Gushee, D. E. 1996. Stratospheric ozonedepletion: Regulatory issues. Congr. Res.Serv. Issue Brief. No. IB89021.

27. Hamaker, P., De Heer, H., and Van der Burg,A. M. M. 1983. Use of gas tight plastic filmsduring fumigation of glasshouse soils withmethyl bromide. II. Effects on the bromide-ion mass balance for a polder district. ActaHortic. 152:127-135.

28. Hartz, T. K., DeVay, J. E., and Elmore, E. L.1993. Solarization is an effective soil disin-festation technique for strawberry production.HortScience 28:104-106.

29. Katan, J. 1981. Solar heating (solarization) ofsoil for control of soil-borne pests. Annu.Rev. Phytopathol. 19:211-236.

30. Larkin, R. P., and Fravel, D. R. 1995. Bio-control of Fusarium wilt disease. Proc. Annu.Int. Conf. Methyl Bromide Alternatives Emis-sions.

31. Liebman, J. 1994. Alternatives to methylbromide in California strawberry production.IPM Practitioner 16:1-12.

32. Lobert, J. M., Butler, J. H., Montzka, S. A.,Geller, L., Myers, R., and Elkins, J. W. 1995.A net sink for atmospheric methyl bromide inthe east Pacific Ocean. Science 267:1002-1005.

33. Lumsden, R. D., Lewis, J. A., and Fravel, D.R. 1993. Formulation and delivery of biocon-trol agents for use against soilborne plantpathogens. Pages 166-182 in: Biorational PestControl Agents: Formulation and Delivery. F.R. Hall and J. W. Barry, eds. AmericanChemical Society, Washington, DC.

34. Lynch, L. M. 1996. Agricultural Trade and

Jean B. Ristaino

Dr. Ristaino is an associate professor in the Department of Plant Pathology at NorthCarolina State University. She earned a B.S. in biological sciences with a botanyemphasis in 1979 and an M.S. in plant pathology from the University of Maryland in1982. She worked in the Soilborne Diseases Laboratory, USDA, Beltsville, from 1982 to1984. She earned her Ph.D. in plant pathology from the University of California, Davis,in 1987. She joined the faculty at North Carolina State University in October 1987. Herresearch has focused primarily on the ecology and epidemiology of soilborne plantpathogens, including Phytophthora species on pepper, potato, tomato, and soybean,and Sclerotium rolfsii on vegetable crops. A major goal of her work is to developecologically based disease management practices that reduce our reliance on pesti-cides. Dr. Ristaino was the 1993 recipient of the outstanding researcher award from the NorthCarolina State University Chapter of Sigma Xi and currently serves as president-elect of theNCSU Chapter. She served as an American Association for the Advancement of ScienceSummer Environmental Policy Fellow in Washington, DC, and worked in the Office ofAtmospheric Programs on the methyl bromide issue. She will teach a graduate courseon “Agriculture, Ethics, and the Environment” in the fall of 1998.

William Thomas

Mr. Thomas is currently the director of the EPA Methyl Bromide Program in the Officeof Atmospheric Programs, Division of Stratospheric Protection. He focuses on thephaseout of methyl bromide due to its ozone-depleting qualities and primarily assistscurrent methyl bromide users in finding environmentally sound and economically viablealternatives to this pesticide. He has been with the EPA since 1992, working on themethyl bromide issue. From 1990 to 1992, he worked with the U.S. Department ofAgriculture on detail to the Agency for International Development (USAID), workingon African environmental issues. From 1987 to 1990, he worked in West Africa withUSAID on Desert Locus control. Prior to this, he was with the Peace Corps in theWest African country of Mauritania. His academic background includes a B.S. inAgriculture from the University of Arizona in 1981 and an M.S. in entomology in 1985from the same institution.


Environmental Concerns: Three Essays Ex-ploring Pest Control, Regulations, and Envi-ronmental Issues. Ph.D. Diss. University ofCalifornia, Berkeley.

35. Maas, J. L., Galletta, G. J., and Draper, A. D.1989. Resistance in strawberry to races ofPhytophthora fragariae and to isolates ofVerticillium from North America. Acta Hortic.265:521-526.

36. MacDonald, J. 1996. Control of Fusarium wiltof carnation by soil heating processes. Proc.1996 Annu. Int. Conf. Methyl Bromide Alter-natives Emission Reductions.

37. Marois, J. J., Dunn, M. T., and Papavizas, G.C. 1983. Reinvasion of fumigated soil byFusarium oxysporum f. sp. melonis. Phyto-pathology 73:680-684.

38. Maw, G. A., and Kempton, R. J. 1973. Methylbromide as a soil fumigant. Soil Fert. 36:41-47.

39. Mellouki, A., Talukdar, R. K., Schmoltner, A.,Gierczak, T., Mills, M. J., Solomon, S., andRavishankara, A. R. 1992. Atmospheric life-times and ozone depletion potentials ofmethyl bromide and dibromomethane. Geo-phys. Res. Lett. 19:2059-2062.

40. Menge, J. A., Munnecke, D. E., Johnson, E.L. V., and Carnes, D. W. 1978. Dosage re-sponse of the vesicular-arbuscular mycorrhi-zal fungi Glomus fasciculatus and G. con-strictus to methyl bromide. Phytopathology68:1368-1372.

41. Molina, M. J., and Rowland, F. S. 1974.Stratospheric sink for chlorofluoromethanes:Chlorine atom catalyzed destruction of ozone.Nature 249:810-812.

42. Montzka, S. A., Butler, J. H., Myers, R. C.,Thompson, T. M., Swanson, T. H., Clarke, A.D., Lock, L. T., and Elkins, J. 1996. Declinein the tropospheric abundance of halogenfrom halocarbons: Implications for strato-

spheric ozone depletion. Science 272:1318-1322.

43. Morrissey, W. A. 1996. Methyl Bromide andStratospheric Ozone Depletion: New Direc-tions for Regulation. Congressional ResearchService Report for Congress. No. 96-474SPR.

44. Munnecke, D. E., and Van Gundy, S. D. 1979.Movement of fumigants in soil, dosage re-sponses, and differential effects. Annu. Rev.Phytopathol. 17:405-429.

45. National Oceanic and Atmospheric Admini-stration. 1996. Northern Hemisphere WinterSummary: Selected Indicators of Strato-spheric Climate. National Weather Service,National Center for Environmental Prediction,Climate Prediction Center, Washington, DC.

46. National Research Council. 1996. Ecologi-cally-Based Pest Management. NationalAcademy Press, Washington, DC.

47. Ohr, H. D., Sims, J. J., Grech, N. M., Becker,J. O., and McGiffen, M. E., Jr. 1996. Methyliodide, an ozone-safe alternative to methylbromide as a soil fumigant. Plant Dis. 80:731-735.

48. Opperman, C. H., Taylor, C. G., andConkling, M. A. 1994. Root-knot specificnematode directed expression of a plant rootspecific gene. Science 263:221-223.

49. Oremland, R. S., Miller, L. G., andStrohmaler, F. E. 1994. Degradation of methylbromide in anaerobic sediments. Environ. Sci.Technol. 28:514-520.

50. Pease, W. S., Robinson, J. C., and Tuden, D.1996. Taxing pesticides to fund environ-mental protection and IPM. California PolicySeminar Report, University of California,Berkeley.

51. Penkett, S. A., Jones, B. M. R., Rycroft, M. J.,and Simmons, D. A. 1985. An interhemi-

spheric comparison of the concentrations ofbromine compounds in the atmosphere. Na-ture 318:550-553.

52. Pimentel, D., Acquay, H., Biltonen, M., Rice,P., Silva, M., Nelson, J., Lipner, V., Giordano,S., Horowitz, A., and D’Amore, M. 1992. En-vironmental and Economic Costs of PesticideUse. Bioscience 42:750-760.

53. Ragsdale, N. N., and Wheeler, W. B. 1995.Methyl bromide: Risks, benefits, and currentstatus in pest control. Pages 21-44 in: Reviewof Pesticide Toxicology. R. M. Roe and R. J.Kuhr, eds. Toxic Communication Inc., Ra-leigh, NC.

54. Ristaino, J. B., Parra, G., and Campbell, C. L.1997. Suppression of Phytophthora blight inbell pepper by a no-till wheat cover crop.Phytopathology 87:242-249.

55. Ristaino, J. B., Perry, K. B., and Lumsden, R.D. 1991. Effect of solarization and Gliocla-dium virens on sclerotia of Sclerotium rolfsii,soil microbiota, and the incidence of southernblight of tomato. Phytopathology 81:1117-1124.

56. Ristaino, J. B., Perry, K. B., and Lumsden, R.D. 1996. Soil solarization and Gliocladiumvirens reduce the incidence of southern blightin bell pepper in the field. Biocontrol Sci.Tech. 6:583-593.

57. Robock, A. 1996. Stratospheric control ofclimate. Science 272:972-973.

58. Shorter, J. H., Kolb, C. E., Crill, P. M., Ker-win, R. A., Talbot, R. W., Hines, M. E., andHarriss, R. C. 1995. Rapid degradation of at-mospheric methyl bromide in soils. Nature377:717-719.

59. Singh, H. B., and Kanakidou, M. 1993. Aninvestigation of the atmospheric sources andsinks of methyl bromide. Geophys. Res. Lett.20:133-136.

An advertisement appears in the printed journal in this space.


60. Slaper, H., Velders, G. J. M., Daniel, J. S., deGruijl, F. R, and van der Leun, J. 1996. Esti-mates of ozone depletion and skin cancer in-cidence to examine the Vienna Conventionachievements. Nature 384:256-258.

61. Solomon, S., Mills, M., Heidt, L. E., Pollock,W. H., and Tuck, A. F. 1992. On the evalua-tion of ozone depletion potential. J. Geophys.Res. 97:825-842.

62. Spreen, T. H., Van Sickle, J. J., Moseley, A.E., Deepak, M. S., and Mathers, L. 1995. Useof methyl bromide and the economic impactof its proposed ban on the Florida fresh mar-ket fruit and vegetable industry. Bull. Univ.Fla. Exp. Stn. No. 898.

63. Stapleton, J., and DeVay, J. E. 1986. Soilsolarization: A nonchemical approach formanagement of plant pathogens and pests.Crop Prot. 5:190-198.

64. Stolarski, R., Bojkov, R., Bishop, L., Zerefos,C., Staehelin, J., and Zawodny, J. 1992.Measured trends in stratospheric ozone. Sci-ence 256:342-349.

65. Taylor, R. W. D. 1994. Methyl bromide: Isthere any future for this noteworthy fumigant?J. Stor. Prod. Res. 30:253-260.

66. Thomas, W. 1996. Alternatives to MethylBromide. Vol. 2. Ten Case Studies. Soil,Commodity, and Structural Use. U.S. Envi-ronmental Protection Agency, Spec. Publ.430-R-96-021.

67. United Nations Environment Programme.1992. Montreal Protocol Assessment Supple-ment, Methyl Bromide: Its Science, Technol-ogy, and Economics. Synthesis Report of theMethyl Bromide Interim Scientific Assess-ment and Methyl Bromide Interim Technol-ogy and Economic Assessment.

68. United Nations Environment Programme.1995. 1994 Report of the Methyl BromideTechnical Options Committee. Montreal Pro-tocol on Substances that Deplete the OzoneLayer. United Nations Ozone Secretariat, Nai-

robi, Kenya. 69. United States Department of Agriculture.

1993. The Biologic and Economic Assess-ment of Methyl Bromide. National Agricul-tural Pesticide Impact Assessment Program.U.S. Dep. Agric. Rep., April 1993.

70. United States Department of Agriculture.1995. Agricultural Chemical Usage: 1994Vegetable Summaries. National AgriculturalStatistics Service, Economic Research Serv-ice, Washington, DC. No. Ag Ch 1 (95).

71. United States Environmental ProtectionAgency. 1993. 40 CFR Part 82, Protection ofStratospheric Ozone: Final Rule. FederalRegister, v 58, no. 236, Dec. 10, 1993. 65018-65062.

72. United States Government Accounting Office.1995. Pesticides: The Phaseout of MethylBromide in the United States. GAO/RCED-96-16, Washington, DC.

73. United States International Trade Commis-sion. 1996. Fresh tomatoes from Mexico. In-vestigation number 731-TA-747. Publ. No.2967.

74. van Bruggen, A. H. C. 1995. Plant diseaseseverity in high-input compared to reduced-input and organic farming systems. Plant Dis.79:976-984.

75. Winterbottom, C., Westerlund, F., Mircetich,J., Galpa, L., and Welch, N. 1996. Evaluationof relative resistance of different strawberrycultivars to Phytophthora and Verticilliumdahliae as a potential alternative to methylbromide. Pages 36-1 to 35-5 in: Proc. 1996Annu. Int. Conf. Methyl BromideAlternatives Emission Reductions.

76. Workneh, F., van Bruggen, A. H. C., Drink-water, L. E., and Shennan, C. 1993. Variablesassociated with corky root and Phytophthoraroot rot of tomatoes in organic and conven-tional farms. Phytopathology 83:581-589.

77. World Meteorological Organization. 1994.Scientific Assessment of Ozone Depletion:

1994. Global Ozone Research and MonitoringProject No. 37, Geneva.

78. Wu, Y., Perry, K., and Ristaino, J. B. 1996.Estimating temperature of mulched and baresoil from meteorological data. J. Agric. For.Meteor. 81:299-323.

79. Yagi, K., Williams, J., Wang, N. Y., andCicerone, R. J. 1993. Agricultural soil fumi-gation as a source of atmospheric methylbromide. Proc. Natl. Acad. Sci. 90:8420-8423.

80. Yarkin, C., Sunding, D., Zilberman, D., andSiebert, J. 1994. All crops should not betreated equally. Calif. Agric. 48:10-15.

81. Yarkin, C., Sunding, D., Zilberman, D., andSiebert, J. 1994. Canceling methyl bromidefor postharvest use to trigger mixed-economicresults. Calif. Agric. 48:16-21.

82. Yates, S. R., Ernst, F. F., Gan, J., Gao, F., andYates, M. V. 1996. Methyl bromide emissionsfrom a covered field. II. Volatilization. J. En-viron. Qual. 25:192-202.

83. Yates, S. R., Gan, J., Ernst, F. F., Mutziger, A.,Yates, M. V. 1996. Methyl bromide emissionsfrom a covered field. I. Experimental condi-tions and degradation in soil. J. Environ.Qual. 25:184-192.

84. Yeates, G. W. 1996. Nematode ecology. Rus.J. Nematol. 4:71-75.

85. Yeates, G. W., Bamforth, S. S., Ross, D. J.,Tate, K. R., and Sparling, G. P. 1991. Recolo-nization of methyl bromide sterilized soilsunder four different field conditions. Biol.Fert. Soils 11:181-189.

86. Yuen, G., Schroth, M. N., Weinhold, A. R.,and Hancock, J. G. 1991. Effects of soil fumi-gation with methyl bromide and chloropicrinon root health and yield of strawberry. PlantDis. 75:416-420.

87. Zilberman, D., Schmitz, A., Casterline, G.,Lichtenberg, E., and Siebert, J. B. 1991. Theeconomics of pesticide use and regulation.Science 253:518-522.

Documents

Agriculture, Methyl Bromide, and the Ozone Hole: Can We Fill the … · 2020. 9. 23. · have occurred (64). The ozone holes of 1992 and 1993 were the most severe on record (24,77)