the role of bioherbicides in weed management corresponding author: e-mail: [email protected] the...

* Corresponding author: E-mail: [email protected]

The Role of Bioherbicides in Weed Management

ROBERT J. KREMER*U.S. Department of Agriculture, Agricultural Research Service, Cropping Systems and Water Quality

Research Unit and Department of Soil, Environmental and Atmospheric Sciences, University ofMissouri, Columbia MO 65211, USA

Biopestic. Int. 1(3,4): 127-141 (2005)

ABSTRACT The bioherbicide approach to weed management involves the inundative use ofselected microorganisms for attacking specific weeds and controlling their infestations withinthe same year of application. Ideally, bioherbicides are most effective for weed management inannual cropping systems that are unsuitable for the classical biological control approach,which involve the use of natural enemies requiring more than one year to develop effective,weed suppressive populations. Only a few bioherbicides are successful in field-scale controlof weeds while the effectiveness of other candidate bioherbicides has been limited by restrictedhost-range, elaborate formulation requirements, and lack of persistence in the field. Specialsituations in which bioherbicides may be most effective include management of weeds that areconsidered herbicide-resistant, parasitic, and invasive. Based on the current status of bioherbicideuse, strategies for widening host ranges, improving formulations for practical use, and improvingtechniques for enhancement of weed-suppressive activity in conventional and sustainableagricultural systems are needed if bioherbicides are to make significant contributions to non-chemical weed management.

KEY WORDS : Weed biological control, biotic agents, weed-suppressive microorganisms;deleterious rhizobacteria

INTRODUCTION

Biological control of weeds is the intentionaluse of living organisms (biotic agents) to reduce thevigor, reproductive capacity, density, or impact ofweeds (Quimby and Birdsall, 1995). The strategiesof biological control can be classified in two broadcategories: (i) classical or inoculative, and (ii)inundative or mass exposure. The classical strategyis based on introduction of host-specific organisms(insects, pathogens, nematodes) from the weed’snative range into regions where the weed hasestablished and become a widespread problem. Thebiotic agents, after quarantine to assure hostspecificity, are released into weed-infested sites and

are allowed to adapt and flourish in their new habitatover time to eventually establish a self-perpetuatingregulation of the weed infestation at acceptable levels.Thus, classical biological control requires a timeperiod of one to several years to achieve adequatecontrol while the agent population builds up to levelsto impact the weed population.

The inundative strategy attempts to overwhelma weed infestation with massive numbers of a bioticagent in order to attain weed control in the year ofrelease. In contrast to classical biological control,inundation involves timing of agent release tocoincide with weed susceptibility to the agent andformulation of the agent to provide rapid attack ofthe weed host. A development of the inundative

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strategy is the bioherbicide approach, which involvesapplication of weed pathogens in a manner similarto herbicide applications. Since most bioherbicideshave been developed using selected plantpathogenic fungi that cause such diseases on weedsas anthracnose and rust, the term mycoherbicide isoften used in reference to these fungal preparations.

The objectives of this review are to identify theplace for bioherbicides in weed managementincluding their integration into current systems, todevelop an understanding of factors affecting theirsuccessful use in both conventional and alternativemanagement systems, and to assess the prospectsof developing strategies for using bioherbicides inbiologically-based weed management.

CURRENT STATUS OF BIOHERBICIDEDEVELOPMENT AND USE

Several selected microorganisms have beenextensively evaluated and developed or are underdevelopment for commercial application (Table 1). Thediscovery, development, practical application, andcommercialization of early mycoherbicides (i.e.,‘Collego’, ‘Devine’, ‘Biomal’) have been thoroughlydescribed (Charudattan, 1991; TeBeest, 1996). Theearly mycoherbicides consisted of highly virulentfungal plant pathogens that infected the aerial portionsof weed hosts resulting in visible disease symptoms.These fungi could also be mass cultured in artificialmedia to produce large quantities of inocula needed forfield application. Microbial agents comprising morerecent bioherbicides can include obligate fungalparasites, soil-borne fungal pathogens, non-phytopathogenic fungi, pathogenic and non-pathogenic bacteria, and nematodes. Many of theseorganisms have different cultural and applicationrequirements compared to the early mycoherbicides.This presents a curious dilemma in that even thoughthe number of potential bioherbicides and targetweeds in diverse habitats has expanded over the past25 years, the production and formulation requirementsand application methods have become more complex.This is a disadvantage for developing productionfacilities devoted to bioherbicides because standardculturing and processing techniques cannot be usedin the preparation of the various biological controlagents necessary for attacking several target weeds

that typically infest crop production fields.Unfortunately, production systems for bioherbicides,especially mycoherbicides, will continue to followempirical processes illustrated by evaluation ofcandidate pathogens on a case-by-case basis(Charudattan, 2001).

The bioherbicides listed in Table 1 includeorganisms that have been extensively evaluated forcommercial development including several that haveundergone field testing and evaluation as requiredby regulatory agencies. The original bioherbicide ormycoherbicide concept was based on mass artificialculture of organisms to obtain large quantities ofinoculum for inundative application to the weed hostto achieve rapid epidemic buildup and high levels ofdisease (Charudattan, 1991). Because many of therecent bioherbicide candidates differ from the originaldefinition in requirements for mass production andapplication, the bioherbicide concept has been re-defined as living products that control specific weedsin agricultural systems within a specific, shorttimeframe (Hallet, 2005). The following illustrates thediversity of microorganisms currently in use orundergoing testing by describing selected examplesof production and application of recent bioherbicides.

Most mycoherbicides consist of fungalpathogens such as the Colletotrichum species ableto exist saprophytically in the absence of the planthost, which is important in developing artificialculture strategies for production of inocula. However,some fungal pathogens are obligate parasites thatcan only proliferate directly on host plants. Suchis the case of the rust fungus Puccinia canaliculata,a foliar pathogen of yellow nutsedge (Cyperusesculentus), that is cultured en masse on the weedhost planted in small field plots or greenhousesfrom which uredospores are vacuum-harvested andstored in bulk prior to preparation of themycoherbicide ‘Dr. Biosedge’ (Phatak et al., 1983).The harvested uredospores can be applied in thefield through center-pivot irrigation systems. Themycoherbicide ‘Eco-Clear’, containing the fungalpathogen Chondrostereum purpureum, must beapplied to wounded branches or stumps of weedytree species to inhibit re-sprouting by enhancingdecay of the woody tissues (Prasad, 1996).

2005 Kremer : Biopesticides in Weed Management 129


Soilborne fungi have become importantbioherbicide candidates because these fungi areapplied directly to soils to reduce weed populationsthrough decay of seeds prior to emergence or killseedlings shortly after emergence (Jones andHancock, 1990). Trichoderma virens inoculated incomposted chicken manure significantly reducedbroadleaf and grass weeds in horticultural crops(Héraux et al., 2005a). Plant pathogenic bacteriaincluding Xanthomonas campestris pv poannua(Xcp) and Pseudomonas syringae pv tagetis (Pst),were developed as bioherbicides for control of annualbluegrass (Poa annua) and Asteraceae (composite)weeds, respectively (Johnson et al., 1996). The Xcpbioherbicide (‘Camperico’) must be applied byspraying the bacterial suspension while mowing toallow bacterial cells to invade wounded tissue of thegrass (Imaizumi et al., 1997). The Pst bioherbicide isprepared with organosilicone surfactant to enhancebacterial infection of leaf and stem tissue and onsetof disease.

Deleterious rhizobacteria (DRB) are bacteria thatdiffer from bacterial pathogens based on their non-parasitic nature and ability to aggressively colonizeplant roots and suppress plant growth withoutinvading the root tissues (Kremer and Kennedy, 1996;Kremer, 2006). The DRB are under intensiveinvestigation for bioherbicidal potential.Pseudomonas fluorescens D7 is a soil-applied DRBbioherbicide formulated as a liquid suspension orencapsulated in clay that effectively suppressesdowny brome (Bromus tectorum) in cereal grain crops(Kennedy et al., 1991). Selected DRB formulated assemolina flour granules suppressed velvetleaf(Abutilon theophrasti) seedling growth (Zdor et al.,2005) and root growth of leafy spurge (Euphorbiaesula) established in field infestations (Brinkman etal., 1999). Mechanically-transmitted viruses (i.e.,Tobacco Mild Green Mosaic Virus), produced onsurrogate host plants, harvested, and freeze-dried,are under investigation as bioherbicides of invasiveweeds including tropical soda apple (Solanumviarum) (Charudattan, 2001). Plant-specificnematodes have been reared and formulated forpreliminary evaluation for wide-scale management ofthe rangeland weed, Russian knapweed (Acroptilonrepens) (Caesar-Thon That et al., 1995).

LIMITING FACTORS OF BIOHERBICIDEADOPTIONS AND USE

Factors of narrow host range, specificrequirements for culturing and formulation to assurebiotic agent efficacy, and possible by-products ofpotent mammalian and avian toxins by some fungalagents have limited commercial development ofbioherbicides because of their likely low marketpotential.

Enhancing Host Range of BioherbicidesSuccessful incorporation of bioherbicides into

conventional agriculture will only be achieved if theyare able to effectively and consistently suppressmultiple weeds of economic importance on a verylarge scale (Charudattan, 1990). Currently, the use ofa bioherbicide to control one species in a mixture ofweeds in the field is questionable if a producer hasthe option of a broad-spectrum herbicide to controlmultiple weed species. Fungal pathogens of the samespecies containing strains or subspecies with activityagainst several weeds might be developed throughselective screening or through genetic recombinationor hybridization into broad host-range pathotypesfor use against multiple weed targets (Charudattan,1990; Sands and Pilgeram, 2001). These are long-term tactics, however, as intense evaluation will berequired to meet stringent regulations beforeapproval is granted for release of genetically-alteredorganisms into the environment.

Alternatives to genetic manipulation forimproving the spectrum of weeds controlled includeusing a “multiple-pathogen strategy” andmanipulating the formulation to aid infectiveness ofthe pathogen (Charudattan, 2001). For example, amixture of three pathogens, Drechslera gigantia,Exserohilum longirostratum, and Exserohilumrostratum, which were isolated from three differenthost weeds, successfully suppressed growth ofseven weeds of citrus groves in Florida(Chandramohan and Charudattan, 2003). The multiple-pathogen strategy also shows promise for controllingweeds in row crops illustrated by the successfulcontrol of eight weedy Amaranthus species insoybean by a mixture of Phomopsis amananthicolaand Microsphaeropsis amaranthi conidialsuspensions (Ortiz-Ribbing and Williams, 2006).


Screening trials of the bacterial pathogen Pstprepared as a post-emergence bioherbicide revealedefficacy on several economically important weeds inthe Asteraceae family including wild sunflower(Helianthus spp.), common cocklebur (Xanthiumstrumarium), common ragweed (Ambrosiaartimisifolia), and Canada thistle (Cirsium arvense)in soybean field trials (Johnson et al., 1996).Amendment of Pst aqueous suspensions withsurfactants to aid the bacteria to efficiently invadeplant leaves broadens the host range when it wasfound that weeds outside the Asteraceae family,green foxtail (Setaria viridis), and velvetleaf(Abutilon theophrasti), were also severely injured.

Formulation of BioherbicidesMany of the foliar and stem fungal pathogens

require specific levels of humidity (dew periods) andtemperature for full effectiveness, which necessitatesdevelopment of special formulations to assureeffectiveness after delivery of the agent in the field.Boyetchko et al. (1998) outlined the factors that mustbe addressed in bioherbicide formulation technologyin order to maintain or enhance efficacy of thebiocontrol agent as well as to be compatible withconventional field application systems. The maintypes of formulations currently in use include variousemulsions, organosilicone surfactants, hydrophilicpolymers, and alginate-, starch-, or celluloseencapsulated granules, all of which have advantagesand disadvantages in promoting virulence andefficacy of the biotic agents and ease of application(Charudattan, 2001; Hallett, 2005). The primaryfunctions of the formulation should includepredisposal of the weed to infection by the pathogenand protection of the infecting pathogen againstenvironmental constraints while promoting diseasedevelopment (Charudattan, 2001).

Potential Health Risks of BioherbicidesSome mycoherbicides exhibit strong herbicidal

activity against a range of economically importantweeds, however, the fungal pathogens may alsoproduce undesirable mammalian and avian toxins.Myrothecium verrucaria is highly effective incontrolling a number of weeds through productionof herbicidal metabolites during infection of the hostplant; however, mammalian-toxic macrocyclic

tricothecenes are simultaneously produced, therebypresenting a human health hazard (Anderson andHallet, 2005). Similarly, tricothecenes are producedby the fungal pathogen Fusarium tumidum, understudy as a potential bioherbicide for gorse (Ulexeuropaeus) and broom (Cytisus scoparius) in NewZealand (Morin et al., 2000). Hallet (2005) suggeststhat fungal pathogens that produce both herbicidalmetabolites and mammalian toxins must be fullyinvestigated to assess their role and risks as potentialbioherbicides.

BIOHERBICIDES IN CONVENTIONALCROPPING SYSTEMSConventional cropping systems are characterized aslarge-scale production enterprises that utilize high-yielding crop varieties generally in monoculture orshort term rotations planted on the most fertile,productive soils available with large, costly inputsof chemical fertilizers and pesticides. Theintroduction and rapid adoption of genetically-modified (GM) varieties of the major crops (soybean,maize, cotton, canola) that are resistant to herbicidesallow control of a broad spectrum of weeds with asingle herbicide. Conventional cropping systemsusing either GM or non-GM crop varieties are basedon the seasonal use of herbicides to reduce weedinfestations to acceptable levels so that crops canbe grown profitably with little consideration of a morelong-term approach for weed management. Despitethe advancements in herbicide technology anddevelopment of GM herbicide-resistant crops,surveys continue to indicate that farmers perceiveannual and perennial weed infestations as the mostserious crop pest problem that affect their enterprises(Aref and Pike, 1998; Gibson et al., 2005). Thesefindings suggest that many farmers might considerincorporating alternative, effective, nonchemicalweed control methods into their overall weedmanagement plans.

Despite limitations of current bioherbicides,chemical herbicide use will level off and possiblydecrease in importance due to social andenvironmental concerns, development of herbicide-resistant weed biotypes, and reduced availability ofnew, environmentally compatible herbicides whileemphasis on “biologically-based pest management”


will increase. Bioherbicides may be effective inconventional cropping systems under severalcircumstances including: (i) weeds evolved resistanceto a broad-spectrum herbicide; (ii) excessive rates ofherbicides are required to control one weed species(bioherbicides would allow less herbicide use); (iii)parasitic weeds are not controlled due to lack ofselective herbicides; (iv) herbicides cannot be useddue to cost or environmental limitations; and (v)invasive weed species become established and fewherbicide options are available (Kremer, 2002).

Bioherbicides and Herbicide-resistant WeedsAlthough management of the multiple-weed

complex in row crops may be addressed in the shortterm through use of herbicide-resistant transgeniccrops, herbicide-resistant weed biotypes willeventually develop after repeated applications of thesame herbicide in a given field. For example,glyphosate-resistant rigid ryegrass (Lolium rigidum)developed after repeated applications of glyphosatein an orchard to control grass weeds (Powles et al.,1998). Even more serious is the development of weedbiotypes with resistance to multiple herbicides thatare widely used in row crop production. Foes et al.(1998) reported a biotype of common waterhemp(Amaranthus rudis), a major weed in maize andsoybean in the Midwestern U.S., with resistance totwo widely-used herbicides. Also, a downy bromebiotype was characterized with resistance to eightchemically dissimilar herbicides (Park and Mallory-Smith, 2005). As herbicide resistance becomes moreproblematic with many common weeds, strategiesusing bioherbicides will become more important inmaintaining adequate weed control in conventionalsystems. The potential for successful use ofbioherbicides in managing herbicide-resistantbiotypes was demonstrated where growth of animazaquin-resistant common cocklebur biotypeoriginating in soybean fields was suppressed withthe mycoherbicide, Alternaria helianthi (Abbas andBarrentine, 1995).

Bioherbicides and Parasitic WeedsMany crop production regions throughout the

world are infested with parasitic weeds that attackspecific crop plants causing drastic yield reduction.There are no selective herbicides for satisfactorily

controlling parasitic weeds; therefore, bioherbicidescould be potentially highly effective on these weeds.Indeed, some of the most recent successfulbioherbicides have been for control of dodders(Cuscuta spp.) in soybean and cranberry (Table 1).Also, a soil fungus under evaluation suppressesgermination and attachment of witchweed (Strigasp.) seedlings to grain sorghum roots, contributingto grain yield increases (Ciotola et al., 1995).Development of this pathogen as a biotic agent couldhave significant impacts on food production inregions where Striga spp. are dominant weedproblems. Recently, a strategy for selectingrhizosphere bacteria or fungi that inhibit broomrape(Orobanche spp.) germination and infection ofhorticultural crops by overproducing amino acids hasbeen proposed as an effective bioherbicidalapproach (Vurro et al., 2006).

Bioherbicides and Developing Weed ProblemsBioherbicides may also have a place in weed

species that have not yet reached a competitivethreshold level. An example might be their useagainst perennial weeds that are increasing underreduced-tillage farming systems. Shifts in weedcomposition in response to changes in croppingpractices, such as tillage, result in developmentof sub-competitive populations during the earlyyears of the shift. The general tendency is forperennial species to increase as the amount oftillage decreases. For example, common milkweed(Asclepias syriaca) infestations increased in theMidwestern United States in response to continueduse of reduced tillage. Although common milkweedtypically infested wheat, corn, and soybeans underreduced or no-tillage, it probably only slightlyreduced crop yields (Aldrich and Kremer, 1997).Bioherbicides might provide a way of keeping thisweed from becoming an economically importantweed in the future. The discovery of a bacterialdisease affecting common milkweed (Flynn andVidaver, 1995) may lead to the development of thecausal agent, Xanthomonas campestris pv.asclepiadis, as a biotic agent for maintenance ofcommon milkweed infestations below economicthreshold levels. The disease is a systemic blightand reduces overall plant vigor and stand density.The report of milkweed bacterial blight is significantbecause a practical “preventive biological control


approach” can be developed and because discoveryof similar agents on other perennial weeds for whichno options for chemical control is possible.

Bioherbicides may have an important role inmanaging invasive weeds, defined as those alienplants spreading naturally in natural ecosystems andproducing significant changes in terms ofcomposition, structure, or ecosystem processes(Masters and Sheley, 2001). Invasive weeds are anemerging management challenge because from aneconomic or agricultural productivity perspectivemost are not undesirable but are considered verydisruptive from an ecological and conservationstandpoint. Many of the weeds inhabitingrangelands, forests, and riparian areas as listed inTable 1 may be considered invasive weeds. Althoughclassical biological control strategies may be mostappropriate for these situations, some bioherbicidesdeveloped for weeds in these habitats have shownpromise in effective control. The phytopathogenicbacterium Pseudomonas syringae pv. phaseolicolawas shown to suppress growth of the invasive weedkudzu (Pueraria lobata) (Zidack and Backman, 1996).Anderson and Gardner (1999) have demonstrated thepotential of Ralstonia solanacearum as biologicalcontrol agent of alien kahili ginger (Hedychiumgardnerianum), and invasive weed in tropical forestecosystems. Bioherbicides will be of significant valuein managing weeds in areas where herbicides are noteffective due to regulations that severely restrict orprohibit herbicide use and where a primarymanagement goal is preservation of the environment.These special situations include restoration of nativeecosystems, wetlands, national parks, wildliferefuges, and areas bordering waterways (riparianborders). For example, red alder (Alnus rubra) is aforest weed that interferes with timber production inthe Pacific West forest region of Canada. Red alderinfestations can be suppressed using biocontrolfungi that are inoculated into woody stems withinjecting devices (Dorworth, 1995). Thismycoherbicide is useful for control of red alder alongstreams, where herbicide application is prohibited, bycausing a “slow kill” and allowing simultaneousrelease of nutrients from dying vegetation for use bydesirable tree species as well as gradual re-populationof the site by the timber trees.

BIOHERBICIDES IN INTEGRATED WEEDMANAGEMENT

An expanded and long-term approach to weedcontrol is integrated weed management in which allavailable strategies including tillage, culturalpractices, herbicides, allelopathy, and biologicalcontrol are used to reduce the weed seedbank insoil, prevent weed emergence, and minimizecompetition from weeds growing with desired plants(Aldrich and Kremer, 1997). Like chemical herbicides,bioherbicides may be most effective as a componentin an overall management program rather than as asingle tactic approach. This may be the mostpromising situation for bioherbicides as a practicalmanagement option in cropping systems. Whenconsidered as a three-part system, weed managementoffers several opportunities for integration ofbioherbicides at critical stages during weeddevelopment: as seeds in soil, as growing andcompetitive plants, and during seed production(Aldrich and Kremer, 1997).

Integrating Bioherbicides with Chemical HerbicidesSeveral scenarios for integrating bioherbicides

into weed management programs can be developed(Table 2). Because most biological control agentsare specific toward one weed and most productionfields contain several predominant weed species, theuse of bioherbicides for control of a single speciesin conjunction with herbicides selected for controlof other weeds present is a logical approach.Compatibility of the bioherbicide Fusarium solani f.sp. cucurbitae, which controls Texas gourd(Cucurbita texana), a problem weed in soybean andcotton in the southern United States, demonstratedthat it could be integrated into a weed managementstrategy to broaden the spectrum of weed controlwithin the crop (Weidemann and Templeton, 1988).

Integration with reduced rates of herbicides cansuccessfully improve activity of mycoherbicidestoward weeds. For example, Phoma proboscis wasmore effective in controlling field bindweed(Convolvulus arvensis) when combined with sub-lethal doses of 2,4-D than when applied alone (Heiny,1994). Application of either of three herbicides atone-fourth rate with a sub-lethal dose of thepathogen Pyricularia setariae achieved complete


control of green foxtail, which demonstrated apathogen-herbicide synergy (Peng and Byer, 2005).The fungus Colletotrichum gloeosporioides f. sp.malvae, endemic on round-leaved mallow, adequatelycontrols this weed (about 75% kill) when appliedalone as a bioherbicide (Grant et al., 1990). Severalchemical herbicides are only effective on round-leafedmallow in the early seedling stage. Combinations ofthe bioherbicide with several herbicides atrecommended rates were evaluated for post-emergence control at the 4- to 5-leaf stage of growth.Tank mixtures of the fungus with either metribuzin orimazethapyr greatly enhanced control and reducedbiomass production over the fungus or the herbicidealone. These results clearly demonstrate that in somecases no single method is adequate for weed controland that combinations of methods are most effective.

Integrating Bioherbicides with Cultural PracticesCultural practices offer convenient application

methods for integrating bioherbicides in croppingsystems. Crop rotation is a practice that may also bemanipulated to encourage development of specificinhibitory bacteria on roots. Tillage can influencethe frequency of inhibitory bacteria occurring in soiland their growth-suppressing activity. Greaterproportions of indigenous rhizobacteria inhibitory todowny brome and jointed goatgrass were detectedunder either conventional or reduced tillagecompared to no-till. This finding suggests thatapplication of selected DRB during tillage may beeffective in integrated weed management (Kremerand Kennedy, 1996). Vegetative residues at or nearthe soil surface could serve as substrates forproduction of weed-suppressive chemicals by DRBapplied as bioherbicides directly to the residues.Previous work reporting a rotation effect in corn wasdue partly to certain rhizobacteria specificallyassociated with corn roots illustrates the potentialfor using DRB to achieve suppression of weeds incrop rotation systems (Turco et al., 1990). Increasingcrop interference in the field by manipulating rowspacing, seeding rates and other cultural practicesto suppress early weed growth has been proposedas a viable component of integrated weedmanagement (Jordan, 1993). Selection of highlycompetitive and allelopathic soybean varieties (Roseet al., 1984) and matched with compatible

bioherbicides may provide early-season weedsuppression and require only minimal subsequentpost-emergence weed control.

Bioherbicide and Management of Seed Banks andSeedlings

Prevention of seed germination and seedlingemergence is fundamental to maximal effective, long-term weed management (Aldrich and Kremer, 1997).Thus, bioherbicides can play a significant role inreducing weed infestations by attacking seeds andseedlings before they become competitive with cropplants. Several approaches for managing the seedbank and seedling emergence have been describedincluding direct application of biotic agents to soilor crop residues (Begonia et al., 1998), or to cropseeds to prevent emergence of weeds in the cropseed-germination zone (Kremer, 2000), and incombination with solarization for enhancing seeddeterioration in soils (Kremer and Kennedy, 1996).Also, certain agrochemicals that stimulate seedimbibition or germination can be combined withbioherbicides containing selected seed-attackingmicroorganisms, incorporated into soil, and killgerminating weed seeds (Kremer and Schulte, 1989).

Sustainable Agricultural SystemsCrop production enterprises that avoid or restrict

the use of chemical herbicides both in productionfields and in environmentally-sensitive areas favorthe adoption of bioherbicides. For simplicity,sustainable agriculture encompasses similar systemsknown as alternative, natural, organic, biological,ecological, and biodynamic farming. The sustainableagricultural systems involve a range of technologicaland management options to reduce costs, protecthealth and environmental quality, and enhancebeneficial biological interactions and naturalprocesses (National Research Council, 1989). Innearly all cases, little, if any, synthetic chemicals(including herbicides) are used. Thus, sustainableagricultural systems provide the greatestopportunities to study, refine, and implement non-chemical weed management (Liebman and Gallandt,1997) that will yield valuable information fordeveloping improved bioherbicides and advancingtheir use in broader biologically-based weedmanagement systems. Because the demand for


bioherbicides for sustainable agriculture andecosystem management is currently small relative tochemical herbicides, such products may be providedmost efficiently through small-scale, specializedindustries or even on-farm production facilitiesfocused on “niche markets” (Auld and Morin, 1995;Charudattan, 1990; Hallet, 2005)

Bioherbicides and Biological Weed ManagementBioherbicides may be most effective in managing

weeds as a component in a biological weedmanagement system that is associated withsustainable agriculture. Biological weed managementinvolves the use of diversity of biological agentssuch as bioherbicides and other biopesticides, andbiological approaches including allelopathy, cropcompetition, and other cultural practices to obtainsimilar dramatic reduction in weed densities oftenassociated with herbicide use (Cardina, 1995).Examples of biological weed management approachesare listed in Table 2. Because some sustainableagricultural systems demand pesticide-free cropproduction (i.e., organic farming), the approach toweed control resembles a biological weedmanagement system in which bioherbicides are majorcomponents. Many of the approaches are similar tothose for integrated weed management except thatherbicides are not involved. Therefore, bioherbicidesthat would not be used in conventional integratedweed management because of unacceptable efficacyor too much time required for realization of effectswould be under practical use in biological weedmanagement. For example, prevention of weed seedproduction and reduction of the seed bank could beattained using a bioherbicide consisting of seedpathogens applied to weeds infesting the crop(Medd and Campbell, 1996). However, the impact ofthe bioherbicide would not be evident for one totwo years when noticeable decreases in weedseedling densities occur due to reduced weed seedpopulations in the soil.

Cover crops and mulches as components ofsustainable management systems may be used forintegrating bioherbicides by delivering the agentson seeds and promoting their establishment in soilsfor attack on weed seeds and seedlings prior toplanting the main crop. Recent research demonstratedthat several cover crop species inoculated with a

DRB bioherbicide at planting maintained DRBpopulations on their roots and in the rhizospherethereby promoting root colonization of giant foxtail(Setaria faberi) seedlings that emerged early in thegrowing season of the main crop after the cover cropswere terminated (Kremer, 2000). Combined effects ofthe DRB and allelopathic activity of the cover cropresidues suppressed the growth of the weeds.Similarly, a “system management” approach where aspecific weed growing with a crop is sprayed with apost-emergence bioherbicide and the crop isunderseeded with a living green cover crop hasresulted in successful control of the target weed aswell as the remaining weed flora by the cover crop(Pfirter et al., 1997). Also, agents in formulationapplied at planting can attack weed seeds andseedlings through delivery of bioherbicides to soilby either direct inoculation of crop seeds or bypromoting colonization of crop roots (Skipper et al.,1996). Crop roots not only might deliver microbialagents to adjacent weed roots but may also maintainor even enhance the agents’ numbers for attack ofseedlings emerging later in the season.

In sustainable agricultural systems the use ofsynergisms can be explored in which the combineduse of two or more methods enable bioherbicides tocontrol weeds more effectively than when used alone(Gressel et al., 1996; TeBeest, 1996). Bioherbicideefficacy on hemp sesbania (Sesbania exaltata) wasincreased by combining selected bacteria with thefungal pathogen, Colletotrichum truncatum (Schisleret al., 1991). Combinations of a Colletotrichum sp.bioherbicide with a naturally-occurring rust fungusallowed the bioherbicide to infect the weed host(Xanthium sp.) through rust lesions resulting indeath of the plant (Morin et al., 1993). A seed-feedinginsect combined with seed-attacking fungisignificantly decreased velvetleaf seed viability andseedling emergence and increase seed infectioncompared to either the insect or fungus alone(Kremer and Spencer, 1989). Pre-dispersal seedmortality of weeds escaping herbicide control maybe effective in manipulating and reducing seed banksin soil. A practical application of soil-applieddetrimental bacteria and fungi combined with insectswould be in situations where the insect feeds onroots or crowns of target weeds (Caesar, 2003)


The very nature of high inputs of organicamendments and green manure crops in sustainableagricultural systems promotes the ability of crops tocompete more vigorously with weeds, whichintuitively suggests that efficacy of bioherbicideswould also be enhanced when used with theseamendments (Gallandt et al., 1998). Indeed thebioherbicidal fungus, Trichoderma virens, producedthe phytotoxin viridiol when grown in organicsubstrates such as peat and composts making thisbioherbicide ideal for use in biological weedmanagement (Jones and Hancock, 1990; Héraux andWeller, 2005a). This bioherbicide combined withherbicidal compounds released by a rye cover cropextended weed suppression throughout the growingseason of selected horticultural crops (Héraux et al.,2005b). Furthermore, Trichoderma virens alsoproduces biocidal compounds effective againstfungal plant pathogens, which suggests thepossibility of developing biotic agents with efficacytoward multiple pests.

Sustainable agricultural systems are positionedfor implementation of novel tactics and approachesfor manipulating the field environment to enhancethe activity of indigenous pathogens of weedspresent as natural bioherbicides. This strategy ofweed suppression, also known as “conservationbiological control,” is an ecological concept that hasonly recently received attention from anagroecosystems standpoint. Management activitiesthat affect soil organisms can directly affect weedsas demonstrated with reduced tillage, maintenanceof high soil organic matter, reduced inputs ofagrichemicals, which lead to high populations ofdeleterious soil microorganisms that contribute tonatural weed suppression (Kremer and Li, 2003).Specific examples are limited, however, Lindquist etal. (1995) reported a natural population of the fungalpathogen Verticillium sp. significantly suppressedvelvetleaf growth in soybean under reduced tillage.Additions of composted swine manure to soilinhibited germination and seedling emergence ofthree weed species possibly by enhancing soilborneweed-suppressive microorganisms (Menalled et al.,2005). As pointed out by Hallet (2005), conservationbiological control should not be considered theprimary weed control strategy but should be

investigated as a component of an integrated weedmanagement program.

CONCLUSIONSDespite apparent advances in biological control

as a reliable strategy for weed management, littleprogress has been made in developing tactics forpractical application in agro-ecosystems, especiallythose involving cropping systems. Efficaciousstrategies that target multiple weed species areneeded. Best success in achieving this may wellinvolve selection of several “core strains” of agentsthat are adapted to soils and climates in specificregions and are able to suppress growth of weedscomprising the dominant species at that site. To gainacceptance of these strategies, integration ofbiological control into current management systemsis imperative so that the potential effectiveness ofthe agents can be demonstrated. Bioherbicidestargeted for niche markets and their use insustainable agricultural systems will likelydemonstrate the greatest effectiveness in biologicalweed management in the short term. This will generateimpetus for continued discovery and developmentof bioherbicides for more widespread use. From aweed management standpoint, the integration ofmultiple tactics, including a diversity of potentialbioherbicides and biologically-based approaches,favors the effectiveness and stability required forlong-term weed management (Cardina, 1995).

The integration of biological control intocurrent systems also offers augmentative weedcontrol options, as herbicide use becomes morerestricted. It is well known that continued use ofsingle herbicide control tactics favors resistancedevelopment in certain weed populations andconventional cropping systems. Bioherbicidetechnology used in appropriate integrated weedmanagement in diversified cropping systems may aidin restoring fertility and productivity to degradedecosystems and avoid the buildup of herbicide-resistant and invasive weeds. Bioherbicidesappropriately integrated in agricultural andenvironmental restoration systems can play a majorrole in reclaiming and restoring biodiversity toecosystems degraded through continuousimplementation of conventional cropping systems.


Situations in which environment quality are restoredin both ecologically sound farming systems andnative habitats will benefit from the use of effectivebioherbicides.

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Accepted 20 December 2005

the role of bioherbicides in weed management corresponding author: e-mail: [email protected] the...

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