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 of Missouri, Columbia MO 65211, USA

Biopestic. Int. 1(3,4): 127-141 (2005) ABSTRACT The bioherbicide approach to weed management involves the inundative use of selected for attacking specific weeds and controlling their infestations within the same year of application. Ideally, bioherbicides are most effective for weed management in annual 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 control of weeds while the effectiveness of other candidate bioherbicides has been limited by restricted host-range, elaborate formulation requirements, and lack of persistence in the field. Special situations in which bioherbicides may be most effective include management of weeds that are considered -resistant, parasitic, and invasive. Based on the current status of bioherbicide use, strategies for widening host ranges, improving formulations for practical use, and improving techniques for enhancement of weed-suppressive activity in conventional and sustainable agricultural 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 are allowed to adapt and flourish in their new habitat over time to eventually establish a self-perpetuating Biological control of weeds is the intentional regulation of the weed infestation at acceptable levels. use of living organisms (biotic agents) to reduce the Thus, classical biological control requires a time vigor, reproductive capacity, density, or impact of period of one to several years to achieve adequate weeds (Quimby and Birdsall, 1995). The strategies control while the agent population builds up to levels of biological control can be classified in two broad to impact the weed population. categories: (i) classical or inoculative, and (ii) The inundative strategy attempts to overwhelm inundative or mass exposure. The classical strategy a weed infestation with massive numbers of a biotic is based on introduction of host-specific organisms agent in order to attain in the year of (insects, pathogens, nematodes) from the weed’s release. In contrast to classical biological control, native range into regions where the weed has inundation involves timing of agent release to established and become a widespread problem. The coincide with weed susceptibility to the agent and biotic agents, after quarantine to assure host formulation of the agent to provide rapid attack of specificity, are released into weed-infested sites and the weed host. A development of the inundative

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

1-05/0127-0141/©2005 (KRF) 128 International Vol. 1, no. 3,4 strategy is the bioherbicide approach, which involves that typically infest crop production fields. application of weed pathogens in a manner similar Unfortunately, production systems for bioherbicides, to herbicide applications. Since most bioherbicides especially mycoherbicides, will continue to follow have been developed using selected plant empirical processes illustrated by evaluation of pathogenic fungi that cause such diseases on weeds candidate pathogens on a case-by-case basis as anthracnose and rust, the term mycoherbicide is (Charudattan, 2001). often used in reference to these fungal preparations. The bioherbicides listed in Table 1 include The objectives of this review are to identify the organisms that have been extensively evaluated for place for bioherbicides in weed management commercial development including several that have including their integration into current systems, to undergone field testing and evaluation as required develop an understanding of factors affecting their by regulatory agencies. The original bioherbicide or successful use in both conventional and alternative mycoherbicide concept was based on mass artificial management systems, and to assess the prospects culture of organisms to obtain large quantities of of developing strategies for using bioherbicides in inoculum for inundative application to the weed host biologically-based weed management. to achieve rapid epidemic buildup and high levels of disease (Charudattan, 1991). Because many of the CURRENT STATUS OF BIOHERBICIDE recent bioherbicide candidates differ from the original DEVELOPMENT AND USE definition in requirements for mass production and Several selected microorganisms have been application, the bioherbicide concept has been re- extensively evaluated and developed or are under defined as living products that control specific weeds development for commercial application (Table 1). The in agricultural systems within a specific, short discovery, development, practical application, and timeframe (Hallet, 2005). The following illustrates the commercialization of early mycoherbicides (i.e., diversity of microorganisms currently in use or ‘Collego’, ‘Devine’, ‘Biomal’) have been thoroughly undergoing testing by describing selected examples described (Charudattan, 1991; TeBeest, 1996). The of production and application of recent bioherbicides. early mycoherbicides consisted of highly virulent Most mycoherbicides consist of fungal fungal plant pathogens that infected the aerial portions pathogens such as the Colletotrichum species able of weed hosts resulting in visible disease symptoms. to exist saprophytically in the absence of the plant These fungi could also be mass cultured in artificial host, which is important in developing artificial media to produce large quantities of inocula needed for culture strategies for production of inocula. However, field application. Microbial agents comprising more some fungal pathogens are obligate parasites that recent bioherbicides can include obligate fungal can only proliferate directly on host plants. Such parasites, soil-borne fungal pathogens, non- is the case of the rust fungus Puccinia canaliculata, phytopathogenic fungi, pathogenic and non- a foliar pathogen of yellow nutsedge (Cyperus pathogenic , and nematodes. Many of these esculentus), that is cultured en masse on the weed organisms have different cultural and application host planted in small field plots or greenhouses requirements compared to the early mycoherbicides. from which uredospores are vacuum-harvested and This presents a curious dilemma in that even though stored in bulk prior to preparation of the the number of potential bioherbicides and target mycoherbicide ‘Dr. Biosedge’ (Phatak et al., 1983). weeds in diverse habitats has expanded over the past 25 years, the production and formulation requirements The harvested uredospores can be applied in the and application methods have become more complex. field through center-pivot irrigation systems. The This is a disadvantage for developing production mycoherbicide ‘Eco-Clear’, containing the fungal facilities devoted to bioherbicides because standard pathogen Chondrostereum purpureum, must be culturing and processing techniques cannot be used applied to wounded branches or stumps of weedy in the preparation of the various biological control tree species to inhibit re-sprouting by enhancing agents necessary for attacking several target weeds decay of the woody tissues (Prasad, 1996). 2005 Kremer : Biopesticides in Weed Management 129 130 Biopesticides International Vol. 1, no. 3,4

Soilborne fungi have become important LIMITING FACTORS OF BIOHERBICIDE bioherbicide candidates because these fungi are ADOPTIONS AND USE applied directly to soils to reduce weed populations Factors of narrow host range, specific through decay of seeds prior to emergence or kill requirements for culturing and formulation to assure seedlings shortly after emergence (Jones and biotic agent efficacy, and possible by-products of Hancock, 1990). Trichoderma virens inoculated in potent mammalian and avian toxins by some fungal composted chicken manure significantly reduced agents have limited commercial development of broadleaf and grass weeds in horticultural crops bioherbicides because of their likely low market (Héraux et al., 2005a). Plant pathogenic bacteria potential. including Xanthomonas campestris pv poannua (Xcp) and Pseudomonas syringae pv tagetis (Pst), Enhancing Host Range of Bioherbicides were developed as bioherbicides for control of annual Successful incorporation of bioherbicides into bluegrass (Poa annua) and Asteraceae (composite) conventional agriculture will only be achieved if they weeds, respectively (Johnson et al., 1996). The Xcp are able to effectively and consistently suppress bioherbicide (‘Camperico’) must be applied by multiple weeds of economic importance on a very spraying the bacterial suspension while mowing to large scale (Charudattan, 1990). Currently, the use of allow bacterial cells to invade wounded tissue of the a bioherbicide to control one species in a mixture of grass (Imaizumi et al., 1997). The Pst bioherbicide is weeds in the field is questionable if a producer has prepared with organosilicone surfactant to enhance the option of a broad-spectrum herbicide to control bacterial infection of leaf and stem tissue and onset multiple weed species. Fungal pathogens of the same of disease. species containing strains or subspecies with activity Deleterious rhizobacteria (DRB) are bacteria that against several weeds might be developed through differ from bacterial pathogens based on their non- selective screening or through genetic recombination parasitic nature and ability to aggressively colonize or hybridization into broad host-range pathotypes plant roots and suppress plant growth without for use against multiple weed targets (Charudattan, invading the root tissues (Kremer and Kennedy, 1996; 1990; Sands and Pilgeram, 2001). These are long- Kremer, 2006). The DRB are under intensive term tactics, however, as intense evaluation will be investigation for bioherbicidal potential. required to meet stringent regulations before Pseudomonas fluorescens D7 is a soil-applied DRB approval is granted for release of genetically-altered bioherbicide formulated as a liquid suspension or organisms into the environment. encapsulated in clay that effectively suppresses Alternatives to genetic manipulation for downy brome (Bromus tectorum) in cereal grain crops improving the spectrum of weeds controlled include (Kennedy et al., 1991). Selected DRB formulated as using a “multiple-pathogen strategy” and semolina flour granules suppressed velvetleaf manipulating the formulation to aid infectiveness of (Abutilon theophrasti) seedling growth (Zdor et al., the pathogen (Charudattan, 2001). For example, a 2005) and root growth of leafy spurge (Euphorbia mixture of three pathogens, Drechslera gigantia, esula) established in field infestations (Brinkman et Exserohilum longirostratum, and Exserohilum al., 1999). Mechanically-transmitted viruses (i.e., rostratum, which were isolated from three different Tobacco Mild Green Mosaic Virus), produced on host weeds, successfully suppressed growth of surrogate host plants, harvested, and freeze-dried, seven weeds of citrus groves in Florida are under investigation as bioherbicides of invasive (Chandramohan and Charudattan, 2003). The multiple- weeds including tropical soda apple (Solanum pathogen strategy also shows promise for controlling viarum) (Charudattan, 2001). Plant-specific weeds in row crops illustrated by the successful nematodes have been reared and formulated for control of eight weedy Amaranthus species in preliminary evaluation for wide-scale management of soybean by a mixture of Phomopsis amananthicola the rangeland weed, Russian knapweed (Acroptilon and Microsphaeropsis amaranthi conidial repens) (Caesar-Thon That et al., 1995). suspensions (Ortiz-Ribbing and Williams, 2006). 2005 Kremer : Biopesticides in Weed Management 131

Screening trials of the bacterial pathogen Pst tricothecenes are simultaneously produced, thereby prepared as a post-emergence bioherbicide revealed presenting a human health hazard (Anderson and efficacy on several economically important weeds in Hallet, 2005). Similarly, tricothecenes are produced the Asteraceae family including wild sunflower by the fungal pathogen Fusarium tumidum, under (Helianthus spp.), common cocklebur (Xanthium study as a potential bioherbicide for gorse (Ulex strumarium), common ragweed (Ambrosia europaeus) and broom (Cytisus scoparius) in New artimisifolia), and Canada thistle (Cirsium arvense) Zealand (Morin et al., 2000). Hallet (2005) suggests in soybean field trials (Johnson et al., 1996). that fungal pathogens that produce both herbicidal Amendment of Pst aqueous suspensions with metabolites and mammalian toxins must be fully surfactants to aid the bacteria to efficiently invade investigated to assess their role and risks as potential plant leaves broadens the host range when it was bioherbicides. found that weeds outside the Asteraceae family, green foxtail (Setaria viridis), and velvetleaf BIOHERBICIDES IN CONVENTIONAL (Abutilon theophrasti), were also severely injured. CROPPING SYSTEMS Conventional cropping systems are characterized as Formulation of Bioherbicides large-scale production enterprises that utilize high- Many of the foliar and stem fungal pathogens yielding crop varieties generally in monoculture or require specific levels of humidity (dew periods) and short term rotations planted on the most fertile, temperature for full effectiveness, which necessitates productive soils available with large, costly inputs development of special formulations to assure of chemical fertilizers and . The effectiveness after delivery of the agent in the field. introduction and rapid adoption of genetically- Boyetchko et al. (1998) outlined the factors that must modified (GM) varieties of the major crops (soybean, be addressed in bioherbicide formulation technology maize, cotton, canola) that are resistant to in order to maintain or enhance efficacy of the allow control of a broad spectrum of weeds with a biocontrol agent as well as to be compatible with single herbicide. Conventional cropping systems conventional field application systems. The main using either GM or non-GM crop varieties are based types of formulations currently in use include various on the seasonal use of herbicides to reduce weed emulsions, organosilicone surfactants, hydrophilic infestations to acceptable levels so that crops can polymers, and alginate-, starch-, or cellulose be grown profitably with little consideration of a more encapsulated granules, all of which have advantages long-term approach for weed management. Despite and disadvantages in promoting virulence and the advancements in herbicide technology and efficacy of the biotic agents and ease of application development of GM herbicide-resistant crops, (Charudattan, 2001; Hallett, 2005). The primary surveys continue to indicate that farmers perceive functions of the formulation should include annual and perennial weed infestations as the most predisposal of the weed to infection by the pathogen serious crop pest problem that affect their enterprises and protection of the infecting pathogen against (Aref and Pike, 1998; Gibson et al., 2005). These environmental constraints while promoting disease findings suggest that many farmers might consider development (Charudattan, 2001). incorporating alternative, effective, nonchemical Potential Health Risks of Bioherbicides weed control methods into their overall weed Some mycoherbicides exhibit strong herbicidal management plans. activity against a range of economically important Despite limitations of current bioherbicides, weeds, however, the fungal pathogens may also chemical herbicide use will level off and possibly produce undesirable mammalian and avian toxins. decrease in importance due to social and Myrothecium verrucaria is highly effective in environmental concerns, development of herbicide- controlling a number of weeds through production resistant weed biotypes, and reduced availability of of herbicidal metabolites during infection of the host new, environmentally compatible herbicides while plant; however, mammalian-toxic macrocyclic emphasis on “biologically-based pest management” 132 Biopesticides International Vol. 1, no. 3,4 will increase. Bioherbicides may be effective in controlling parasitic weeds; therefore, bioherbicides conventional cropping systems under several could be potentially highly effective on these weeds. circumstances including: (i) weeds evolved resistance Indeed, some of the most recent successful to a broad-spectrum herbicide; (ii) excessive rates of bioherbicides have been for control of dodders herbicides are required to control one weed species (Cuscuta spp.) in soybean and cranberry (Table 1). (bioherbicides would allow less herbicide use); (iii) Also, a soil fungus under evaluation suppresses parasitic weeds are not controlled due to lack of germination and attachment of witchweed (Striga selective herbicides; (iv) herbicides cannot be used sp.) seedlings to grain sorghum roots, contributing due to cost or environmental limitations; and (v) to grain yield increases (Ciotola et al., 1995). invasive weed species become established and few Development of this pathogen as a biotic agent could herbicide options are available (Kremer, 2002). have significant impacts on food production in regions where Striga spp. are dominant weed Bioherbicides and Herbicide-resistant Weeds problems. Recently, a strategy for selecting Although management of the multiple-weed rhizosphere bacteria or fungi that inhibit broomrape complex in row crops may be addressed in the short (Orobanche spp.) germination and infection of term through use of herbicide-resistant transgenic horticultural crops by overproducing amino acids has crops, herbicide-resistant weed biotypes will been proposed as an effective bioherbicidal eventually develop after repeated applications of the approach (Vurro et al., 2006). same herbicide in a given field. For example, glyphosate-resistant rigid ryegrass (Lolium rigidum) Bioherbicides and Developing Weed Problems developed after repeated applications of glyphosate Bioherbicides may also have a place in weed in an orchard to control grass weeds (Powles et al., species that have not yet reached a competitive 1998). Even more serious is the development of weed threshold level. An example might be their use biotypes with resistance to multiple herbicides that against perennial weeds that are increasing under are widely used in row crop production. Foes et al. reduced-tillage farming systems. Shifts in weed (1998) reported a biotype of common waterhemp composition in response to changes in cropping practices, such as tillage, result in development (Amaranthus rudis), a major weed in maize and of sub-competitive populations during the early soybean in the Midwestern U.S., with resistance to years of the shift. The general tendency is for two widely-used herbicides. Also, a downy brome perennial species to increase as the amount of biotype was characterized with resistance to eight tillage decreases. For example, common milkweed chemically dissimilar herbicides (Park and Mallory- (Asclepias syriaca) infestations increased in the Smith, 2005). As herbicide resistance becomes more Midwestern United States in response to continued problematic with many common weeds, strategies use of reduced tillage. Although common milkweed using bioherbicides will become more important in typically infested wheat, corn, and soybeans under maintaining adequate weed control in conventional reduced or no-tillage, it probably only slightly systems. The potential for successful use of reduced crop yields (Aldrich and Kremer, 1997). bioherbicides in managing herbicide-resistant Bioherbicides might provide a way of keeping this biotypes was demonstrated where growth of an weed from becoming an economically important imazaquin-resistant common cocklebur biotype weed in the future. The discovery of a bacterial originating in soybean fields was suppressed with disease affecting common milkweed (Flynn and the mycoherbicide, Alternaria helianthi (Abbas and Vidaver, 1995) may lead to the development of the Barrentine, 1995). causal agent, Xanthomonas campestris pv. asclepiadis, as a biotic agent for maintenance of Bioherbicides and Parasitic Weeds common milkweed infestations below economic Many crop production regions throughout the threshold levels. The disease is a systemic blight world are infested with parasitic weeds that attack and reduces overall plant vigor and stand density. specific crop plants causing drastic yield reduction. The report of milkweed bacterial blight is significant There are no selective herbicides for satisfactorily because a practical “preventive biological control 2005 Kremer : Biopesticides in Weed Management 133

approach” can be developed and because discovery BIOHERBICIDES IN INTEGRATED WEED of similar agents on other perennial weeds for which MANAGEMENT no options for chemical control is possible. An expanded and long-term approach to weed Bioherbicides may have an important role in control is integrated weed management in which all managing invasive weeds, defined as those alien available strategies including tillage, cultural plants spreading naturally in natural ecosystems and practices, herbicides, allelopathy, and biological producing significant changes in terms of control are used to reduce the weed seedbank in composition, structure, or ecosystem processes soil, prevent weed emergence, and minimize (Masters and Sheley, 2001). Invasive weeds are an competition from weeds growing with desired plants emerging management challenge because from an (Aldrich and Kremer, 1997). Like chemical herbicides, economic or agricultural productivity perspective bioherbicides may be most effective as a component most are not undesirable but are considered very in an overall management program rather than as a disruptive from an ecological and conservation single tactic approach. This may be the most standpoint. Many of the weeds inhabiting promising situation for bioherbicides as a practical rangelands, forests, and riparian areas as listed in management option in cropping systems. When Table 1 may be considered invasive weeds. Although considered as a three-part system, weed management classical biological control strategies may be most offers several opportunities for integration of appropriate for these situations, some bioherbicides bioherbicides at critical stages during weed developed for weeds in these habitats have shown development: as seeds in soil, as growing and promise in effective control. The phytopathogenic competitive plants, and during seed production bacterium Pseudomonas syringae pv. phaseolicola (Aldrich and Kremer, 1997). was shown to suppress growth of the invasive weed kudzu (Pueraria lobata) (Zidack and Backman, 1996). Integrating Bioherbicides with Chemical Herbicides Anderson and Gardner (1999) have demonstrated the Several scenarios for integrating bioherbicides potential of Ralstonia solanacearum as biological into weed management programs can be developed control agent of alien kahili ginger (Hedychium (Table 2). Because most biological control agents gardnerianum), and invasive weed in tropical forest are specific toward one weed and most production ecosystems. Bioherbicides will be of significant value fields contain several predominant weed species, the in managing weeds in areas where herbicides are not use of bioherbicides for control of a single species effective due to regulations that severely restrict or in conjunction with herbicides selected for control prohibit herbicide use and where a primary of other weeds present is a logical approach. management goal is preservation of the environment. Compatibility of the bioherbicide Fusarium solani f. These special situations include restoration of native sp. cucurbitae, which controls Texas gourd ecosystems, wetlands, national parks, wildlife (Cucurbita texana), a problem weed in soybean and refuges, and areas bordering waterways (riparian cotton in the southern United States, demonstrated borders). For example, red alder (Alnus rubra) is a that it could be integrated into a weed management forest weed that interferes with timber production in strategy to broaden the spectrum of weed control the Pacific West forest region of Canada. Red alder within the crop (Weidemann and Templeton, 1988). infestations can be suppressed using biocontrol Integration with reduced rates of herbicides can fungi that are inoculated into woody stems with successfully improve activity of mycoherbicides injecting devices (Dorworth, 1995). This toward weeds. For example, Phoma proboscis was mycoherbicide is useful for control of red alder along more effective in controlling field bindweed streams, where herbicide application is prohibited, by (Convolvulus arvensis) when combined with sub- causing a “slow kill” and allowing simultaneous lethal doses of 2,4-D than when applied alone (Heiny, release of nutrients from dying vegetation for use by 1994). Application of either of three herbicides at desirable tree species as well as gradual re-population one-fourth rate with a sub-lethal dose of the of the site by the timber trees. pathogen Pyricularia setariae achieved complete 134 Biopesticides International Vol. 1, no. 3,4 control of green foxtail, which demonstrated a bioherbicides may provide early-season weed pathogen-herbicide synergy (Peng and Byer, 2005). suppression and require only minimal subsequent The fungus Colletotrichum gloeosporioides f. sp. post-emergence weed control. malvae, endemic on round-leaved mallow, adequately controls this weed (about 75% kill) when applied Bioherbicide and Management of Seed Banks and alone as a bioherbicide (Grant et al., 1990). Several Seedlings chemical herbicides are only effective on round-leafed Prevention of seed germination and seedling mallow in the early seedling stage. Combinations of emergence is fundamental to maximal effective, long- the bioherbicide with several herbicides at term weed management (Aldrich and Kremer, 1997). recommended rates were evaluated for post- Thus, bioherbicides can play a significant role in emergence control at the 4- to 5-leaf stage of growth. reducing weed infestations by attacking seeds and Tank mixtures of the fungus with either metribuzin or seedlings before they become competitive with crop imazethapyr greatly enhanced control and reduced plants. Several approaches for managing the seed biomass production over the fungus or the herbicide bank and seedling emergence have been described alone. These results clearly demonstrate that in some including direct application of biotic agents to soil cases no single method is adequate for weed control or crop residues (Begonia et al., 1998), or to crop and that combinations of methods are most effective. seeds to prevent emergence of weeds in the crop seed-germination zone (Kremer, 2000), and in Integrating Bioherbicides with Cultural Practices combination with solarization for enhancing seed Cultural practices offer convenient application deterioration in soils (Kremer and Kennedy, 1996). methods for integrating bioherbicides in cropping Also, certain agrochemicals that stimulate seed systems. Crop rotation is a practice that may also be imbibition or germination can be combined with manipulated to encourage development of specific bioherbicides containing selected seed-attacking inhibitory bacteria on roots. Tillage can influence microorganisms, incorporated into soil, and kill the frequency of inhibitory bacteria occurring in soil germinating weed seeds (Kremer and Schulte, 1989). and their growth-suppressing activity. Greater proportions of indigenous rhizobacteria inhibitory to Sustainable Agricultural Systems downy brome and jointed goatgrass were detected Crop production enterprises that avoid or restrict under either conventional or reduced tillage the use of chemical herbicides both in production compared to no-till. This finding suggests that fields and in environmentally-sensitive areas favor application of selected DRB during tillage may be the adoption of bioherbicides. For simplicity, effective in integrated weed management (Kremer sustainable agriculture encompasses similar systems and Kennedy, 1996). Vegetative residues at or near known as alternative, natural, organic, biological, the soil surface could serve as substrates for ecological, and biodynamic farming. The sustainable production of weed-suppressive chemicals by DRB agricultural systems involve a range of technological applied as bioherbicides directly to the residues. and management options to reduce costs, protect Previous work reporting a rotation effect in corn was health and environmental quality, and enhance due partly to certain rhizobacteria specifically beneficial biological interactions and natural associated with corn roots illustrates the potential processes (National Research Council, 1989). In for using DRB to achieve suppression of weeds in nearly all cases, little, if any, synthetic chemicals crop rotation systems (Turco et al., 1990). Increasing (including herbicides) are used. Thus, sustainable crop interference in the field by manipulating row agricultural systems provide the greatest spacing, seeding rates and other cultural practices opportunities to study, refine, and implement non- to suppress early weed growth has been proposed chemical weed management (Liebman and Gallandt, as a viable component of integrated weed 1997) that will yield valuable information for management (Jordan, 1993). Selection of highly developing improved bioherbicides and advancing competitive and allelopathic soybean varieties (Rose their use in broader biologically-based weed et al., 1984) and matched with compatible management systems. Because the demand for 2005 Kremer : Biopesticides in Weed Management 135 136 Biopesticides International Vol. 1, no. 3,4 bioherbicides for sustainable agriculture and DRB bioherbicide at planting maintained DRB ecosystem management is currently small relative to populations on their roots and in the rhizosphere chemical herbicides, such products may be provided thereby promoting root colonization of giant foxtail most efficiently through small-scale, specialized (Setaria faberi) seedlings that emerged early in the industries or even on-farm production facilities growing season of the main crop after the cover crops focused on “niche markets” (Auld and Morin, 1995; were terminated (Kremer, 2000). Combined effects of Charudattan, 1990; Hallet, 2005) the DRB and allelopathic activity of the cover crop residues suppressed the growth of the weeds. Bioherbicides and Biological Weed Management Similarly, a “system management” approach where a Bioherbicides may be most effective in managing specific weed growing with a crop is sprayed with a weeds as a component in a biological weed post-emergence bioherbicide and the crop is management system that is associated with underseeded with a living green cover crop has sustainable agriculture. Biological weed management resulted in successful control of the target weed as involves the use of diversity of biological agents well as the remaining weed flora by the cover crop such as bioherbicides and other biopesticides, and (Pfirter et al., 1997). Also, agents in formulation biological approaches including allelopathy, crop applied at planting can attack weed seeds and competition, and other cultural practices to obtain seedlings through delivery of bioherbicides to soil similar dramatic reduction in weed densities often by either direct inoculation of crop seeds or by associated with herbicide use (Cardina, 1995). promoting colonization of crop roots (Skipper et al., Examples of biological weed management approaches 1996). Crop roots not only might deliver microbial are listed in Table 2. Because some sustainable agents to adjacent weed roots but may also maintain agricultural systems demand -free crop or even enhance the agents’ numbers for attack of production (i.e., ), the approach to seedlings emerging later in the season. weed control resembles a biological weed management system in which bioherbicides are major In sustainable agricultural systems the use of components. Many of the approaches are similar to synergisms can be explored in which the combined those for integrated weed management except that use of two or more methods enable bioherbicides to herbicides are not involved. Therefore, bioherbicides control weeds more effectively than when used alone that would not be used in conventional integrated (Gressel et al., 1996; TeBeest, 1996). Bioherbicide weed management because of unacceptable efficacy efficacy on hemp sesbania (Sesbania exaltata) was or too much time required for realization of effects increased by combining selected bacteria with the would be under practical use in biological weed fungal pathogen, Colletotrichum truncatum (Schisler management. For example, prevention of weed seed et al., 1991). Combinations of a Colletotrichum sp. production and reduction of the seed bank could be bioherbicide with a naturally-occurring rust fungus attained using a bioherbicide consisting of seed allowed the bioherbicide to infect the weed host pathogens applied to weeds infesting the crop (Xanthium sp.) through rust lesions resulting in (Medd and Campbell, 1996). However, the impact of death of the plant (Morin et al., 1993). A seed-feeding the bioherbicide would not be evident for one to insect combined with seed-attacking fungi two years when noticeable decreases in weed significantly decreased velvetleaf seed viability and seedling densities occur due to reduced weed seed seedling emergence and increase seed infection populations in the soil. compared to either the insect or fungus alone Cover crops and mulches as components of (Kremer and Spencer, 1989). Pre-dispersal seed sustainable management systems may be used for mortality of weeds escaping herbicide control may integrating bioherbicides by delivering the agents be effective in manipulating and reducing seed banks on seeds and promoting their establishment in soils in soil. A practical application of soil-applied for attack on weed seeds and seedlings prior to detrimental bacteria and fungi combined with insects planting the main crop. Recent research demonstrated would be in situations where the insect feeds on that several cover crop species inoculated with a roots or crowns of target weeds (Caesar, 2003) 2005 Kremer : Biopesticides in Weed Management 137

The very nature of high inputs of organic investigated as a component of an integrated weed amendments and green manure crops in sustainable management program. agricultural systems promotes the ability of crops to compete more vigorously with weeds, which CONCLUSIONS intuitively suggests that efficacy of bioherbicides Despite apparent advances in biological control would also be enhanced when used with these as a reliable strategy for weed management, little amendments (Gallandt et al., 1998). Indeed the progress has been made in developing tactics for bioherbicidal fungus, Trichoderma virens, produced practical application in agro-ecosystems, especially the phytotoxin viridiol when grown in organic those involving cropping systems. Efficacious substrates such as peat and composts making this strategies that target multiple weed species are bioherbicide ideal for use in biological weed needed. Best success in achieving this may well management (Jones and Hancock, 1990; Héraux and involve selection of several “core strains” of agents Weller, 2005a). This bioherbicide combined with that are adapted to soils and climates in specific herbicidal compounds released by a rye cover crop regions and are able to suppress growth of weeds extended weed suppression throughout the growing comprising the dominant species at that site. To gain season of selected horticultural crops (Héraux et al., acceptance of these strategies, integration of 2005b). Furthermore, Trichoderma virens also biological control into current management systems produces biocidal compounds effective against is imperative so that the potential effectiveness of fungal plant pathogens, which suggests the the agents can be demonstrated. Bioherbicides possibility of developing biotic agents with efficacy targeted for niche markets and their use in toward multiple pests. sustainable agricultural systems will likely Sustainable agricultural systems are positioned demonstrate the greatest effectiveness in biological for implementation of novel tactics and approaches weed management in the short term. This will generate for manipulating the field environment to enhance impetus for continued discovery and development the activity of indigenous pathogens of weeds of bioherbicides for more widespread use. From a present as natural bioherbicides. This strategy of weed management standpoint, the integration of weed suppression, also known as “conservation multiple tactics, including a diversity of potential biological control,” is an ecological concept that has bioherbicides and biologically-based approaches, only recently received attention from an favors the effectiveness and stability required for agroecosystems standpoint. Management activities long-term weed management (Cardina, 1995). that affect soil organisms can directly affect weeds The integration of biological control into as demonstrated with reduced tillage, maintenance current systems also offers augmentative weed of high soil organic matter, reduced inputs of control options, as herbicide use becomes more agrichemicals, which lead to high populations of restricted. It is well known that continued use of deleterious soil microorganisms that contribute to single herbicide control tactics favors resistance natural weed suppression (Kremer and Li, 2003). development in certain weed populations and Specific examples are limited, however, Lindquist et conventional cropping systems. Bioherbicide al. (1995) reported a natural population of the fungal technology used in appropriate integrated weed pathogen Verticillium sp. significantly suppressed management in diversified cropping systems may aid velvetleaf growth in soybean under reduced tillage. in restoring fertility and productivity to degraded Additions of composted swine manure to soil ecosystems and avoid the buildup of herbicide- inhibited germination and seedling emergence of resistant and invasive weeds. Bioherbicides three weed species possibly by enhancing soilborne appropriately integrated in agricultural and weed-suppressive microorganisms (Menalled et al., environmental restoration systems can play a major 2005). As pointed out by Hallet (2005), conservation role in reclaiming and restoring biodiversity to biological control should not be considered the ecosystems degraded through continuous primary weed control strategy but should be implementation of conventional cropping systems. 138 Biopesticides International Vol. 1, no. 3,4

Situations in which environment quality are restored Caesar, A.J. 2003. Synergistic interaction of soilborne in both ecologically sound farming systems and plant pathogens and root-attacking insects in native habitats will benefit from the use of effective classical biological control of an exotic rangeland bioherbicides. weed. Biol. Contr., 28, 144-153. Caesar, A.J., Rees, N.E., Spencer, N.R., and Quimby, Jr., P.C. (1993) Characterization of Rhizoctonia REFERENCES spp. causing disease of leafy spurge in the Abbas, H.K. and Barrentine, W.L. (1995) Alternaria northern plains. Plant Disease, 77, 681-684. helianthi and imazaquin for control of Caesar-ThonThat, T-C., Dyer, W.E., Quimby, Jr., P.C., imazaquin susceptible and resistant cockleber and Rosenthal, S.S. (1995) Formulation of an (Xanthium strumarium) biotypes. Weed Sci., endoparasitic nematode, Subanguina picridis 43, 425-428. Brzeski, a biological control agent for Russian Aldrich, R.J. and Kremer, R.J. (1997) Principles in knapweed, Acroptilon repens (L.) D.C. Biol. Weed Management, Iowa State University Press, Contr., 5, 262-266. Ames, Iowa, USA. Cardina, J. (1995) Biological weed management. In Aref, S. and Pike, D.R. (1998) Midwest farmers’ A.E. Smith (ed.), Handbook of Weed perception of crop pest infestations. Agronomy Management Systems, Marcel Dekker Inc., New J., 90, 819-925. York, pp. 279-341. Anderson, R.C. and Gardner, D.E. (1999) An Chandramohan, S. and Charudattan, R. (2003) A evaluation of the wilt-causing bacterium multiple-pathogen system for bioherbicidal Ralstonia solanacearum as a potential control of several weeds. Biocontr. Sci. Technol., biological control agent for the alien kahili ginger 13, 199-205. (Hedychium gardnerianum) in Hawaiian forests. Charudattan, R. (1990) Pathogens with potential for Biol. Contr., 15, 89-96. weed control. In R.E. Hoagland (ed.), Microbes Anderson, K.I. and Hallett, S.G. (2004) Herbicidal and Microbial Products as Microbial spectrum and activity of Myrothecium Herbicides, American Chemical Society, verrucaria. Weed Sci., 52, 623-627. Washington, DC, pp. 133-154. Auld, B.A. and Morin, L. (1995) Constraints in the Charudattan, R. (1991) The mycoherbicide approach development of bioherbicides. Weed Technol., to with plant pathogens. In D.O. TeBeest (ed.), 9, 638-652. Microbial Control of Weeds, Chapman & Hall, Bailey, B.A., Hebbar, K.P., Strem, M., Lumsden, R.D., New York, pp. 24-57. Darlington, L.C., Connick, Jr., W.J., and Daigle, Charudattan, R. (2001) Biological control of weeds D.J. (1998) Formulations of Fusarium oxysporum by means of plant pathogens: significance for f.sp. erythroxyli for biocontrol of Erythroxylum integrated weed management in modern agro- coca var. coca. Weed Sci., 46, 682-689. ecology. BioControl, 46, 229-260. Begonia, M.F.T., Kremer, R.J., and Begonia, G.A. Ciotola, M., Watson, A.K., and Hallet, S.G. (1995) (1998) Biological control of weeds: effects of Discovery of an isolate of Fusarium oxysporum rhizobacterial inoculation on the growth of with potential to control Striga hermonthica in velevetleaf (Abutilon theophrasti Medik.). J. Africa. Weed Res., 35, 303-309. Mississippi Acad. Sci., 43, 107-117. Dorworth, C.E. (1995) Biological control of red alder Boyetchko, S., Pederson, E., Punja, Z., and Reddy, (Alnus rubra) with the fungus Nectria ditissima. M. (1998) Formulations of biopesticides. In F.R. Weed Technol., 9, 243-248. Hall and J.J. Menn (eds.), Methods in Flynn, P. and Vidaver, A.K. (1995) Xanthomonas Biotechnology, Vol. 5: Biopesticides: Use and campestris pv. asclepiadis, pv. nov., causative Delivery, Humana Press, Totowa, New Jersey, agent of bacterial blight of milkweed (Asclepias USA, pp. 487-508. spp.). Plant Disease, 79, 1176-1180. Brinkman, M.A., Clay, S.A., and Kremer, R.J. (1999) Foes, M.J., Liu, L., Tranel, P.J., Wax, L.M., and Stoller, Influence of rhizobacteria on leafy spurge E.W. (1998) A biotype of common waterhemp (Euphorbia esula) roots. Weed Technol., 13, (Amaranthus rudis) resistant to triazine and ALS 835-839. herbicides. Weed Sci., 46, 514-520. 2005 Kremer : Biopesticides in Weed Management 139

Gallandt, E.R., Liebman, M., Corson, S., Porter, G.A., Jordan, N. (1993) Prospects for weed control through and Ulrich, S.D. (1998) Effects of pest and soil crop interference. Ecol. Applications, 3, 84-91. management systems on weed dynamics in Julien, M.H. and Griffiths, M.W. (1998) Biological potato. Weed Sci., 46, 238-248. Control of Weeds. A World Catalogue of Agents Grant, N.T., Prusinkiewicz, E., Mortensen, K., and and Their Target Weeds, CAB International, Makowski, R.M.D. (1990) Herbicide interactions Wallingford, UK. with Colletotrichum gloeosporiodes f. sp. malvae, Kennedy, A.C., Elliott, L.F., Young, F.L., and Douglas, a bioherbicide for round leaved mallow (Malva C.L. (1991) Rhizobacteria suppressive to the weed pusilla) control. Weed Technol., 4, 716-723. downy brome. Soil Sci. Soc. Am. J., 55, 722-727. Gibson, K.D., Johnson, W.G., and Hillger, D.E. (2005) Kremer, R.J. (2000) Growth suppression of annual Farmer perceptions of problematic corn and weeds by deleterious rhizobacteria integrated soybean weeds in Indiana. Weed Technol., 19, 1065- with cover crops. In N.R. Spencer (ed.), 1070. Proceedings of the 10th International Gressel, J., Amsellem, Z., Warshawsky, A., Kampel, Symposium on Biological Control of Weeds, V., and Michaeli, D. (1996) Biocontrol of weeds: USDA-ARS and Montana State University, overcoming evolution for efficacy. J. Environ. Bozeman, MT, USA, pp. 931-940. Kremer, R.J. (2002) Bioherbicides: potential successful Sci. Health, B31, 399-405. strategies for weed control. In O. Koul and G.S. Hallet, S.G. (2005) Where are the bioherbicides? Weed Dhaliwal (eds.), Microbial Biopesticides, Taylor Science, 53, 404-415. & Francis, London, pp. 307-323. Héraux, F.M.G., Hallett, S.G., Ragothama, K.G., and Kremer, R.J. (2006) Deleterious rhizobacteria. In S. Weller, S.C. (2005a) Composted chicken manure Gnanamanickam (ed.), Plant-associated as a medium for the production and delivery of Bacteria, Kluwer Academic Publishers, Trichoderma virens for weed control. Dordrecht, Netherlands (in press). HortScience, 40, 1394-1397. Kremer, R.J. and Schulte, L.K. (1989) Influence of Héraux, F.M.G., Hallett, S.G., and Weller, S.C. (2005b) chemical treatment and Fusarium oxysporum on Combining Trichoderma virens-inoculated velvetleaf (Abutilon theophrasti) seed viability. compost and a rye cover crop for weed control in Weed Technol., 3, 369-374. transplanted vegetables. Biol. Contr., 34, 21-26. Kremer, R.J. and Spencer, N.R. (1989) Interaction of insects, Heiny, D.K. (1994) Field survival of Phoma proboscis fungi, and burial on velvetleaf (Abutilon theophrasti) and synergism with herbicides for control field seed viability. Weed Technol., 3, 322-328. bindweed. Plant Disease, 78, 1156-1164. Kremer, R.J. and Kennedy, A.C. (1996) Rhizobacteria Hopen, H.J., Caruso, F.L., Bewick, T.A., Yarborough, as biological control agents of weeds. Weed D.E. and Smagula, J.M. (1997) Control of dodder Technol., 10, 601-609. in Cranberry (Vaccinium macrocarpen) with a Kremer, R.J. and Li, J. (2003) Developing weed- pathogen-based bioherbicide. Acta Hortic., 446, suppressive soils through improved soil quality 427-428. management. Soil Tillage Res., 72, 193-202. Imaizumi, S., Nishino, T., Miyabi, K., Fujimori, T., and Liebman, M. and Gallandt, E.R. (1997) Many little Yamada, M. (1997) Biological control of annual hammers: ecological management of crop-weed bluegrass (Poa annua) with a Japanese isolate interactions. In L.E. Jackson (ed.), Ecology in of Xanthomonas campestris pv. poae (JT-P482). Agriculture, Academic Press, San Diego, CA, Biol. Contr., 8, 7-14. USA, pp. 291-343. Johnson, D.R., Wyse, D.L., and Jones, K.L. (1996) Lindquist, J.L., Maxwell, B.D., Buhler, D.D., and Controlling weeds with phytopathogenic Gunsolus, J.L. (1995) Velvetleaf (Abutilon bacteria. Weed Technol., 10, 621-624. theophrasti) recruitment, survival, seed Jones, R.W. and Hancock, J.G. (1990) Soilborne fungi production and interference in soybean (Glycine for biological control of weeds. In R.E. Hoagland max). Weed Sci., 43, 226-232, (ed.), Microbes and Microbial Products as Masters, R.A. and Sheley, R.L. (2001) Principles and Microbial Herbicides, American Chemical practices for managing rangeland invasive Society, Washington, DC, pp. 276-286. plants. J. Range Manag., 54, 502-517. 140 Biopesticides International Vol. 1, no. 3,4

Medd, R.W. and Campbell, M.A. (1996) A rationale yellow nutsedge with the indigenous rust fungus for the use of a non-specific fungal seed Puccinia canaliculata. Science, 219, 1446-1447. pathogen to control annual grass-weeds of Powles, S.B., Lorraine-Colwill, D.F., Dellow, J.J., and arable lands. In V.C. Moran and G.H. Hoffmann Preston, C. (1998) Evolved resistance to (eds.), Proceedings of the 9th International glyphosate in rigid ryegrass (Lolium rigidum) Symposium on Biological Control of Weeds, in Australia. Weed Sci., 46, 604-607. University of Capetown, Stellenbosch, South Prasad, R. (1996) Development of bioherbicides for Africa, pp. 193-197. integrated weed management in forestry. In H. Menalled, F,D., Buhler, D.D., and Liebman, M. (2005) Brown et al. (eds.), Proceedings of the 2nd Composted swine manure effects on germination International Weed Control Congress, and early growth of crop and weed species Department of Weed Control and Pesticide under greenhouse conditions. Weed Technol., Ecology, Slagelse, Denmark, pp. 1197-1203. 19, 784-789. Quimby, Jr., P.C. and Birdsall, J.L. (1995) Fungal Morin, L., Auld, B.A., and Brown, J.F. (1993) Synergy agents for biological control of weeds: classical between Puccinia xanthii and Colletotrichum and augmentative approaches. In R. Reuveni orbiculare on Xanthium occidentale. Biol. (ed.), Novel Approaches to Integrated Pest Contr., 3, 296-310. Management, CRC Press, Boca Raton, FL, USA, Morin, L., Gianotti, S.F., and Lauren, D.R. (2000) pp. 293-308. Trichothecene production and pathogenicity of Riddle, G.E., Burpee, L.L., and Boland, G.J. (1991) Fusarium tumidum, a candidate bioherbicide for Virulence of Sclerotinia sclerotiorum and S. gorse and broom in New Zealand. Mycol. Res., minor on dandelion (Taraxacum officinale). 104, 993-999. Weed Sci., 39, 109-118. National Research Council (1989) Alternative Rose, S.J., Burnside, O.C., Specht, J.C., and Swisher, Agriculture, National Academy Press, B.A. (1984) Competition and allelopathy between Washington, DC, pp. 448. soybeans and weeds. Agron. J., 76, 523-528. Norman, M.A., Patten, K.D., and Gurusiddaiah, S. Sands, D.C. and Pilgeram, A. (2001) Enhancing the (1994) Evaluation of a phytotoxin(s) from efficacy of biocontrol agents against weeds. Pseudomonas syringae for weed control in In M. Vurro, J. Gressell, T. Burr, G. Harman, R. cranberries. HortScience, 29, 1475-1477. St. Leger, D. Nuss, and A. Pilgeram (eds.), Ortiz-Ribbing, L. and Williams, II, M.M. (2006) Enhancing Biocontrol Agents and Handling Potential of Phomopsis amaranthicola and Risks, IOS, Amsterdam, Netherlands, pp. 3-13. Microsphaeropsis amanthi as bioherbicides for Sands, D.C., Pilgeram, A.L., Zidack, N.K., Jacobsen, several weedy Amaranthus species. Crop Prot., B.J., and Tiourebaev, K.S. (2003) Enhancing the 25, 39-46. efficacy of bioherbicides. In Iacobellis, N.S., Park, K.W. and Mallory-Smith, C.A. (2005) Multiple Collmer, A., Hutcheson, S.W., Mansfield, J.W., herbicide resistance in downy brome (Bromus Morris, C.E., Murillo, J., Schaad, N.W., Stead, tectorum) and its impact on fitness. Weed Sci., D.E., Surico, G., and Ullrich, M.S. (eds.), 53, 780-786. Pseudomonas syringae and Related Pathogens, Peng, G. and Byer, K.N. (2005) Interactions of Kluwer Academic Publishers, Dordrecht, Pyricularia setariae with herbicides for control of Netherlands, pp. 431-441. green foxtail (Setaria viridis). Weed Technol., 19, Schisler, D.A., Howard, K.M., and Bothast, R.J. (1991) 589-598. Enhancement of disease caused by Colletotrichum Pfirter, H.A., Ammon, H.U., Guntli, D., Greaves, M.P., truncatum in Sesbania exaltata by coinoculating and Defago, G. (1997) Towards the management with epiphytic bacteria. Biol. Contr., 1, 261-268. of field bindweed (Convolvulus arvensis) and Skipper, H.D., Ogg, Jr., A.G., and Kennedy, A.C. (1996) hedge bindweed (Calestegia sepium) with fungal Root biology of grasses and ecology of pathogens and cover crops. Integ. Pest Manag. rhizobacteria for biological control. Weed Rev., 2, 61-69. Technol., 10, 610-620. Phatak, S.C., Summer, D.R., Wells, H.D., Bell, D.K., TeBeest, D.O. (1996) Biological control of weeds with and Glaze, N.C. (1983) Biological control of plant pathogens and microbial pesticides. Adv. 2005 Kremer : Biopesticides in Weed Management 141

Agron., 56, 105-113. of Texas gourd, Cucurbita texana, with Turco, R.F., Bischoff, M., Breakwell, D.P., and Griffith, Fusarium solani f. sp. cucrbitae. Weed Technol., D.R. (1990) Contribution of soilborne bacteria 2, 271-274. to the rotation effect in corn. Plant and Soil, Wymore, L.A., Poirier, C., Watson, A.K., and Gotlieb, 122, 115-120. A.R. (1988) Colletotrichum coccodes, a potential Vurro, M., Boari, A., Pilgeram, A.L., and Sands, D.C. bioherbicide for control of velvetleaf (Abutilon (2006) Exogenous amino acids inhibit seed theophrasti). Plant Disease, 72, 534-538. germination and tubercle formation by Zdor, R.E., Alexander, C.M., and Kremer, R.J. (2005) Orobanche ramosa (broomrape): potential Weed suppression by deleterious rhizobacteria application for management of parasitic weeds. is affected by formulation and soil properties. Biol. Contr., 36, 258-265. Commun. Soil Sci. Plant Anal., 36, 1289-1299. Watson, A.K. (1993) Handbook of Biological Zidack, N.K., and Backman, P.A. (1996) Biological Control Agents for Weeds, Weed Science Society control of kudzu (Pueraria lobata) with the plant of America, Champaign, Illinois, USA. pathogen Pseudomonas syringae pv. Weidemann, G.J. and Templeton, G.E. (1988) Control phaseolicola. Weed Sci., 44 645–649.

Accepted 20 December 2005