Bioherbicides are biologically based control agents useful for biological weed control. Hence, bioherbicides have been identified as a significant biological control strategy. Bioherbicides have many advantages such as clearly defined for target weeds, no side effect on beneficial plants or human health, a lack of pesticide residue build-up in the environment, and effectiveness for control of some herbicide-resistant weed biotypes. More importantly, it has been demonstrated that mixtures of some bioherbicides and synthetic herbicides can be more effective. Apart from many bioherbicide benefits, some factors have been noted to restrict the development of bioherbicides into profitable products. They involved environmental, biological and technical–commercial restrictions.
- Bioherbicide (inundative) approach
Development of alternative weed control methods is needed to help decrease reliance on herbicide use. Biological weed control is an alternative option for weed problems, particularly in agriculture and forestry. It is based on the use of natural enemies, particularly insects and pathogens to control weeds, as a sustainable, low cost and more environmentally acceptable method of weed control. One of the approaches to biological weed control using pathogens, mainly fungi, is inundative, bioherbicide approach.
Bioherbicides are phytopathogenic microorganisms or microbial phytotoxins useful for biological weed control applied in similar ways to conventional herbicides [1–3]. The active ingredient in a bioherbicide is, however, a living microorganism. Most commonly the organism is a fungus; hence the term mycoherbicide is often used in these cases . Although the use of fungi and bacteria as inundative biological control agents (bioherbicides) has been recognized as a significant technological weed control alternative [5–9], it can be argued that it serves a more important role as a complementary component in successful integrated management strategies , and not as a replacement for chemical herbicides and other weed management tactics . Actually, in many situations, bioherbicides can be used as the sole option for the management of one or two target weeds, i.e. as a minor supplement to conventional chemical herbicides .
However, according to many authors, bioherbicides offer many advantages in comparison with synthetic herbicides. They include:
a high degree of specificity of target weed;
no effect on non-target and beneficial plants or man;
absence of residue build-up in the environment; and
Except numerous advantages of bioherbicides, some circumstances have been noted to restrain the progress of bioherbicides into profitable outputs. These include:
biological restrictions (host changeability, host scope resistance mechanisms and interaction with other microorganisms that affect efficacy) ;
2. Biological weed control
2.1. Classical (inoculative) approach
The biocontrol approach using an imported pathogen to control a native or naturalized weed with minimal manipulations has been termed the inoculative or classical biocontrol method . The classical approach is directed mainly towards the control of exotic weeds, which have spread in the introduced area in the absence of natural enemies. Control is achieved by the importation and release of highly host-specific pathogens virulent to the target weed in its native region . These agents feed on the weed, reproduce and gradually suppress the weed as their population grows.
A highly successful biological control programme was implemented in Hawaii in the 1970s when a white smut fungus (
Another widely acclaimed example of biological control success is the use of a rust fungus (
Klamathweed beetle (
2.2. Bioherbicide (inundative) approach
Opposite to classical (inoculative) approach, the bioherbicide (inundative) approach uses indigenous plant pathogens that are isolated from weeds and are cultured to produce large quantity of infective material . These are utilized at amounts that will provoke tremendous levels of infection, leading to elimination of the target weed before economic damages happen . A development of this strategy involves application of weed pathogens in a manner similar to herbicide applications. Bioherbicide inoculum is susceptible to unfavourable environmental conditions after spraying, and viability needs to be maintained for as long as is necessary to achieve infection following application . Once in the field, the inundative application of inoculum is timed to coincide with the most favourable environmental conditions and susceptible growth stage of the weed, so that a disease epidemic occurs and the weed population is suppressed [44,45]. Once the weed problem has been removed, natural constraints ensure that the pathogen population returns to a low level once again.
The bioherbicide (inundative) approach has been successfully implemented for a number of important agricultural, invasive and exotic weeds. Many examples dedicated to positive bioherbicide implementation are elaborated in the Section “Bioherbicide case studies”.
3. History of bioherbicides
Utilization of plant pathogens for weed control was first reported in the early 1900s, but the concept of using bioherbicides to control weeds attracted wide interest among weed scientists and plant pathologists after the Second World War. The earliest experiments simply involved fungus
4. Bioherbicide case studies
Considering the research effort expended in this area, some bioherbicides are commercialized (Devine®, Collego®, BioMal®, Camperico®, Myco–TechTM®, Woad Warrior®, Smolder®, Dr. bioSedge®, Biochon®, StampOut® [13,22,28,50–55] and many are underway to develop and register. Plant pathologists and weed scientists have identified approximately 200 plant pathogens that are candidates for development as commercial bioherbicides [48,56]. Some examples are presented below.
Culture filtrates of
5. Interaction between bioherbicides and synthetic herbicides
The idea of combining bioherbicides with synthetic herbicides or adjuvants has been the issue of substantial research work. Moreover, it has been revealed that mixtures of some bioherbicides and synthetic herbicides can be synergistic [85,86], culminating from reduced weed defence reactions caused by the herbicides, consequently making the weeds more sensitive to pathogen attack [87,88]. Christy
6. Bioherbicide limitations
In spite of considerable research in bioherbicides, there are only a few commercially available products worldwide. This lack of availability is mainly due to limitations in bioherbicide development, which need to be overcome to ensure the future commercial success of bioherbicides [22, 101]. Limitations in bioherbicide development can be classified as either environmental (temperature and, particularly, humidity as major factors influencing the efficacy of bioherbicides), biological (mainly host variability and resistance), or technological–commercial (mass production and formulation, which often blocked bioherbicide development) [17,22,102].
7. Environmental limitations
Environmental limitations are a constraint to the effective use of many biological agents, including bioherbicides. Environmental factors influence formulation performance of bioherbicides as inoculum production is dependent on sporulation of the formulation. This process, although rapid, might continue over several weeks subsequent to applications and might encounter variable environmental conditions [18,21,22]. In the application of bioherbicides, environmental conditions prevailing in the phyllosphere of plants are frequently hostile for biological control agents [103,104]. A requirement of more than 12 h of dew period for severe infection by a pathogen has been reported for several potential bioherbicides [105–108] and this may limit the efficacy of the bioherbicide in the field. Temperature generally has not been considered to be as critical as moisture for mycoherbicide , although field efficacy of
Nutrient balance can play an important part in sporulation of fungi. Studies with
Soil environment, moisture and the nutrient status of the soil can influence the physiology of target plants and, therefore, their interaction with aerial applied bioherbicides . Pre-emergence application has been considered as an alternative approach to overcome some of the environmental stresses imposed upon propagules applied onto the foliage or soil surface . Bioherbicides consisting of propagules of soil-borne pathogens, which normally infect at or below the soil surface, appear to be more protected from environmental extremes and may persist and give residual control [116,117]. In this context, Jackson et al.  reported for 95% control of the emerging
There are many environmental limitations to applying bioherbicides and maintaining their efficacy in water as well . Auld and McRae  stated that for control of aquatic weeds a biocontrol agent would need to possess a high ecological capability to contend with varying conditions between surface and bottom, as well as across even small bodies of water. Oxygen concentration, temperature, light intensity and salinity are just four of the variables to contend with.
8. Biological limitations
From a biological viewpoint, a good bioherbicide acts relatively quickly and has acceptable efficacy in control of weeds. Unfortunately, Charudattan  stated that many of the discovered weed pathogens may provide partial control of only one weed species, even under ideal conditions. This host particularity is related to the fundamental bio-physiology of the pathogen and to host changeability [119,120] and resistance as well . In other words, within a population of weed species there will usually be a range of genetically diverse biotypes  that may include some resistant biotypes, just as there may be a range of biotypes of microorganisms , for instance within fungal species, with slightly different host ranges [14,123,124], so that there is potential to mix and vary the biotypes of a species used as a bioherbicide. Non-target plant protection in relation to the potential use of
9. Technological–commercial limitations
Several technological limitations have been identified that could prevent the widespread use of bioherbicides . Pathogenic strains, formulation method and the interaction of these two parameters significantly affect the shelf life of the formulations at room temperature [21,128]. High concentrations and the alteration of formulations are needed to increase bioherbicide activity . Compatibility testing of formulation components that range from registered agricultural products to novel substances, such as sunscreens, humectants and starches, can consume a great deal of time and resources .
The most challenging aspect of formulating bioherbicides is to overcome the dew requirement that exists for several of them. Attempts to overcome this limitation have included developing various water-retaining materials; invert and vegetable oil emulsion formulations [15,94,131] and granular pre-emergence formulations  are considered as a promising approach to make pathogens less dependent on available water for initial infections to occur [133,134]. In addition, appropriate formulations can also reduce the dosage of inoculum required to kill weeds , thus potentially reducing the cost of bioherbicides.
Experiments conducted with a number of potential bioherbicides have demonstrated that an invert emulsion allowed infection to occur in the absence of available water [15,133,136] and reduced the need to apply high dosages of inoculum . Invert emulsions consist of a continuous oil phase that contains water droplets. Connick and Boyette  have developed an invert emulsion formulation exhibiting lower viscosity and greater water-retention properties. Auld  reported that application of low concentrations of vegetable oils with an emulsifying adjuvant enhances efficacy of
From the other side, the main restriction in the application of solid (dry) forms of bioherbicide is that they must await suitable, moist conditions for fungal growth and infection . Moreover, during this waiting period the living active ingredients must survive in the field. In addition, ant theft has been a problem with some formulations .
The simplest liquid formulations of bioherbicides are water suspensions of spores often with a small amount of wetting agent. These are generally used as standards against which to compare more complex formulations. However, under ideal conditions for fungal infection, simple aqueous suspensions can be successful in the field . Pathogenicity of an aqueous mycelial inoculum of
A novel bioherbicide formulation uses a complex emulsion – water-in-oil-in-water (WOW) emulsion . It contains at least one lipophilic surfactant, at least one hydrophilic surfactant, oil and water. Although used in the pharmaceutical , cosmetic  and food industries , WOW emulsions do not appear to have been widely used in agricultural or horticultural technology. Although numerous improvements of liquid formulations of bioherbicides have been made, genetic manipulation of fungi offers a broad extent of opportunities to adjust formulations and to ameliorate bioherbicide characteristics .
Taking into account the above-mentioned restrictions, the production of bioherbicides by profit-oriented companies would involve additional expenditure without guaranteed income. The amount of abundant development and production of phytopathogenic microorganisms or their phytotoxins for bioherbicides in immerse or in solid-state systems, which would alter from one bioherbicide to another, is relatively high . In addition, the small market capacity of considerable competent bioherbicide aspirants reveals that market capacity could be a restraint for developing such herbicides. Because of that, firms are suspicious that development and registration expenditures will be paid back [21,22].
The bioherbicide access to weed control is attaining impetus. New bioherbicides will be applicable in inundate lands, badlands as well as in control of parasite weeds or HR weeds. Research on synergism between pathogens and herbicides for their incorporation in effective weed management, applied science, fungal metabolites and biotechnology utilization, principally genetic engineering is needed. Bioherbicides will not deal with all of the environmental and weed control issues related with synthetic herbicides, nor will they alter the present or future depository of synthetic herbicides. To a certain degree, their appearance will presumably be complementary components in lucrative weed management systems, and in the revelation of different phytotoxins with new performances and new molecular sites of action. Advanced research on this field is imperative in order to entirely find out mutual interactions of phytopathogenic microorganisms, crops and weeds, and to identify new plant pathogens or their phytotoxins promising effective for the new-generation bioherbicides.
Goeden RD. Projects on Biological Control of Russian Thistle and Milk Thistle in California: Failures That Contributed to the Science of Biological Weed Control. In: Spencer N, Noweierski R, Eds. Abstracts of the 10th International Symposium on Biological Control of Weeds. Montana State University, Bozeman, MT, USA; 1999.
Boyetchko SM, Rosskopf EN, Caesar AJ, Charudattan R. Biological Weed Control with Pathogens: Search for Candidates to Applications. In: Khachatourians GG., Arora DK., eds. Applied Mycology and Biotechnology, Vol. 2. Elsevier, Amsterdam; 2002. p239–274.
Boyetchko SM, Peng G. Challenges and Strategies for Development of Mycoherbicides. In: Arora DK., ed. Fungal Biotechnology in Agricultural, Food, and Environmental Applications. Marcel Dekker, New York; 2004. p11–121.
Auld BA, McRae C. Emerging Technologies in Plant Protection - Bioherbicides. Proc. 50th N.Z. Plant Protection Conference 1997; 191–194.
Rosskopf EN, Charudattan R, Kadir JB. Use of Plant Pathogens in Weed Control. In: Katar EH., ed. Handbook of Weed Control. Academic Press, New York, NY; 1999. p891–911.
Boyette CD. The Bioherbicide Approach: Using Phytopathogens to Control Weeds. In: Cobb AH., Kirkwood RC., eds. Herbicides and Their Mechanisms of Action). Sheffield Academic Press, Sheffield, UK; 2000. p134–152.
Charudattan, R. Biological Control of Weeds by Means of Plant Pathogens: Significance for Integrated Weed Management in Modern Agro-ecology. Biocontrol 2001;46(2) 229–260.
Charudattan, R. Ecological, Practical, and Political Inputs into Selection of Weed Targets: What Makes A Good Biological Control Target? Biological Control 2005a; 35(3) 183–196.
Hoagland RE. Microbial Allelochemicals and Pathogens as Bioherbicidal Agents. Weed Technology 2001;15(4) 835–857.
Hoagland RE, Weaver MA, Boyette CD. Myrothecium verrucariaFungus; A Bioherbicide and Strategies to Reduce its Non-Target Risks. Allelopathy Journal 2007;19(1) 179–192.
Singh HP, Batish DR, Kohli RK. Handbook of Sustainable Weed Management. Food Products Press. Binghamton, NY; 2006.
Charudattan, R. Use of Plant Pathogens as Bioherbicides to Manage Weeds in Horticultural Crops. Proc. of the Florida State Horticultural Society 2005b; 118: 208–214.
TeBeest DO. In: ed. Microbial Control of Weeds. Chapman and Hall, New York, NY; 1991. p284.
Boyette CD. Host Range and Virulence of Colletotrichum truncatum, A Potential Mycoherbicide for Hemp Sesbania ( Sesbania exaltata). Plant Disease 1991;75(1) 62–64.
Boyette CD, Quimby PC Jr, Bryson CT, Egley GH, Fulgham FE. Biological Control of Hemp Sesbania ( Sesbania exaltata) Under Field Conditions with Colletotrichum truncatumFormulated in an Invert Emulsion. Weed Science 1993;41(3) 497–500.
Abbas HK, Boyette CD. Solid Substrate Formulation of the Mycoherbicide Colletotrichum truncatumfor Hemp Sesbania ( Sesbania exaltata) Control. Biocontrol Science and Technology 2000;10 297–304.
Auld BA, Hetherington SD, Smith HE. Advances in Bioherbicide Formulation. Weed Biology and Management 2003;3(2) 61–67.
Bailey BA, Hebbar PK, Strem M, Lumsden RD, Darlington LC, Connick WJJr., Daigle DJ, Lumsde ,RD. Formulation of Fusarium oxysporumf. Sp. erythroxylifor Biocontrol of Erythroxylum cocavar . coca. Weed Science 1998;46(6) 682–689.
Kempenaar C, Scheepens PC. Dutch Case Studies Showing the Success and Limitations of Biological Weed Control. In: Pallet K., ed. The 1999 Brighton Conference on Weeds. The British Crop Protection Council, Brighton, UK; 1999. 297–302.
Wheeler GS, Center TD. Impact of the Biological Control Agent Hydrellia pakistanae(Dipetra: Ephydridae) on the Submersed Aquatic Weed Hydrilla verticillata(Hydrocharitaceae). Biological Control 2001;21(2) 168–181.
Altman, J, Neate, S, Rovira, AD. Herbicide Pathogens Interaction and Mycoherbicides as Alternative Strategies for Weed Control. In: Hoagland RE., ed., Microbes and Microbial Products as Herbicides (ed. by Hoagland R.E.). ACS Symposium Series 439. American Chemical Society, Washington DC; 1990. p240–259.
Auld BA, Morin L. Constraints in the Development of Bioherbicides. Weed Technology 1995;9(3) 638–652.
Scheepens, PC, Müller-Schärer, H, Kempenaar, C. Opportunities for Biological Weed Control in Europe. Biological Control 2001;46(2) 127–138.
Watson AK. The Classical Approach with Plant Pathogens. In: TeBeest DO., ed. Microbial Control of Weeds. Chapman and Hall. New York, NY; 1991. p3–23.
DeBach P, Rosen D. Biological Control by Natural Enemies. 2nd edition. Cambridge University Press, UK; 1991.
Julien MH. Biological Control of Weeds: A World Catalogue of Agents and Their Target Weeds. CABI, 3rd ed. Wallingford, UK; 1992.
Watson AK. Biological Control of Weed Handbook. Monograph Series 7. Weed Science Society of American, Champaign, IL; 1993.
Kremer RJ. The Role of Bioherbicides in Weed Management. Biopesticides International 2005;1(3-4) 127–141.
Templeton GE. Status of Weed Control with Plant Pathogens. In: Charudattan R., Walker HL., eds. Biological Control of Weeds with Plant Pathogens. John Wiley & Sons, Inc., New York, NY; 1982. p29–44.
Green S, Stewart-Wade SM, Boland GJ, Teshler MP, Liu SH. Formulating Microorganisms for Biological Control of Weeds. In: Boland GJ., Kuykendall LD., eds. Plant–Microbe Interactions and Biological Control. Marcel Dekker, New York, NY; 1998. p249–281.
Yandoc-Ables CB, Rosskopf EN, Charudattan R. 2007. Plant Pathogens at Work: Progress and Possibilities for Weed Biocontrol Classical Versus Bioherbicidal Approach. Plant Health Progress http://www.apsnet.org/publications/apsnetfeatures/Pages/WeedBiocontrolPart1.asx (accepted 3.02.2015)
Green S. A Review of the Potential for the Use of Bioherbicides to Control Forest Weeds in the UK. Forestry 2003;76(3) 285–298.
Trujillo EE, Aragaki M, Shoemaker RA. Infection, Disease Development and Axenic Cultures of Entyloma Compositarum, the Cause of Hamakua Pamakani Blight in Hawaii. Plant Disease 1988;72(4) 355–357.
Morris MJ, Wood AR, den Breeÿen A. Plant Pathogens and Biological Control of Weeds in South Africa: A Review of Projects and Progress during the Last Decade. In: African Entomology Memoir No. 1. Olckers T., Hill MP., eds. Entomolog. Soc. S. Af., Hatfield; 1999. p125–128.
Cullen JM. Bringing the Cost Benefit Analysis of Biological Control of Chondrilla junceaup to Date. In: Proc. of the 6th Int. Symp. on Biol. Control of Weeds, August 19-25, 1984, Vancouver, Canada. In: Delfosse ES., ed. Agriculture Canada, Ottawa, CA; 1985. p145–152.
Baudoin ABAM, Abad RG, Kok LT, Bruckart WL. Field Evaluation of Puccinia carduorumfor Biological Control of Musk Thistle. Biological Control 1993;3(1) 53–60.
Bruckart WL, Politis DJ, Defago G, Rosenthal SS, Supkoff DM. Susceptibility of Carduus, Cirsium, and CynaraSpecies Artificially Inoculated with Puccinia carduorumfrom Musk Thistle. Biological Control 1996;6(2) 215–221.
Luster DG, Berthier YT, Bruckart WL, Hack MA. Post-Release Spread of Musk Thistle Rust Monitored from Virginia to California Using DNA Sequence Information. In: Spencer NR, ed., Proc. of the 10th Int. Symp. on Biol. Control of Weeds, Montana State University, Bozeman; 1999. p75.
Fisher AJ, Aegerter BJ, Gordon TR, Smith L, Woods DM. Puccinia jaceae var. solstitialis teliospore priming on yellow starthistle. Phytopathology. 2009;99(1) 67–72.
Bruckart WL. Supplemental Risk Analysis of Puccinia jaceaevar. solstitialisfor Biological Control of Yellow Starthistle. Biological Control 2006;37(3) 359–366.
Trujillo EE, Kadooka C, Tanimoto V, Bergfeld S, Shishido G, Kawakami G. Effective Biomass Reduction of the Invasive Weed Species Banana Poka by Septoria Leaf Spot. Plant Disease 2001;85(4) 357–361.
Rees NE, Spencer NR, Knutson LV, Fornasari L, Quimby PC, Pemberton RW, Nowierski RM. Leafy Spurge Euphorbia Esula (complex) Spurge family - Euphorbiaceae. In: Rees NE., Quimby EC Jr., Piper GL., Coombs EM., Turner CE., Spencer NR., Knutson LV., eds. Biological control of weeds in the West. Western Society of Weed Science, Bozeman, MT;1995.
Mico M, Shay J. Effect of Flea Beetles ( Aphthona Nigriscutis) on Prairie Invaded by Leafy Spurge ( Euphorbia Esula) in Maintoba. Great Plains Research: A Journal of Natural and Social Sciences 2002;4(1) 167–184.
Templeton GE, Smith RJ, TeBeest DO. Progress and Potential of Weed Control with Mycoherbicides. Review of Weed Science 1986;2 1–14.
Charudattan R. The Mycoherbicide Approach with Plant Pathogens. In: TeBeest DO., ed. Microbial Control of Weeds. Chapman and Hall, New York, NY; 1991. p24–67.
Inman RE. A Preliminary Evaluation of Rumex Rust as a Biological Control Agent for Curly Dock. Phytopathology 1971;61(1) 102–107.
Oehrens E. Biological Control of Blackberry Through the Introduction of the Rust, Phragmidium violaceum, in Chile. FAO Plant Protection Bulletin 1977;25 26–28.
Barton J. Bioherbicides: All in a Day’s Work... For A Superhero. Online. In: What’s New in Biological Control of Weeds? Manaaki Whenua, Landcare Research, New Zealand Ltd, NZ; 2005. p4–6.
El-Sayed W. Biological Control of Weeds with Pathogens: Current Status and Future Trends. Zeitschrift für Pflanzenkrankheiten und Pflanzenschutz - Journal of Plant Diseases and Protection 2005;112(3) 209–221.
Kenney DS. Devine TM – The Way It Was Developed – An Industrialist’s View. Weed Science 1986;34(1) 15–16.
Bowers RC. Commercialization of Collego® – An Industrialist’ View. Weed Science 1986; 34(1) 24–25.
Hoagland RE. Microbes and Microbial Products as Herbicides. In: Hoagland RE., ed. American Chemical Society Symposium Series 439. ACS Books. Washington, DC; 1990. p341.
Imaizumi S, Nishino T, Miyabe K, Fujimori T, Yamada M. Biological Control of Annual Bluegrass ( Poa annuaL.) with a Japanese Isolate of Xanthomonas campestrispv. poae(JT-P482). Biological Control 1997;8(1) 7–14.
Watson AK. Where Did It Go Wrong? Why Is the Concept of Bioherbicide Suffering From Limited Success? VI international Bioherbicide Group Workshop, Canberra, Australia; 2003.
Venne J. Molecular Characterization and Virulence Analysis of Fusarium oxysporumStrains Used in Biological Control against Striga hermonthica. Master thesis, Department of Plant Science Macdonald Campus of McGill University Montréal. Québec, Canada; 2008.
Boyetchko SM. Innovative Applications of Microbial Agents for Biological Weed Control. In: Biotechnological Approaches in Biocontrol of Plant Pathogens. Mukerji KG., ed. Plenum Publishers, New York, NY; 1999. p73–97.
Zhang W. Development of bioherbicides for biological control of cleavers. Alberta Research Council, Canadian Seed Growers, Association Research and Development Funding, Alberta, CA; 1999.
Marley PS, Kroschel J, Elzien A. Host Specificity of Fusarium oxysporumSchlect (Isolate PSM 197), a Potential Mycoherbicide for Controlling Strigaspp. in West Africa. Weed Research 2005;45(6) 407–412.
Dowler C.C. Weed survey – Southern States: Broadleaf Crops Subsection. Proc. of Southern Weed Science Society 1992; 45: 392–407.
Walker HL, Tilley AM. Evaluation of an Isolate of Myrothecium Verucariafrom Sicklepod ( Senna obtusifolia) as a Potential Mycoherbicide Agent. Biological Control 1997;10(2) 104–112.
Yang S, Jong SC. Host Range Determination of Myrothecium verrucariaIsolated from Leafy Spurge. Plant Disease 1995a;79(10) 994–997.
Yang S, Jong SC. Factors Influencing Pathogenicity of Myrothecium verrucoriaIsolated from Euphorbia esulaon Species of Euphorbia. Plant Disease 1995b; 79(10) 998–1002.
Andolfi A, Boari A, Evidente A, Vurro M. Metabolites Inhibiting Germination of Orobanche ramosaSeeds Produced by Myrothecium verrucariaand Fusarium compactum. Journal of Agricultural and Food Chemistry 2005;53(5) 1598–1603.
Boyette CD, Hoagland RE, Abbas HK. Evaluation of the Bioherbicide Myrothecium verrucaria for Weed Control In Tomato ( Lycopersicon esculentum). Biocontrol Science and Technology 2007;17(2) 171–178.
Rosskopf EN. Evaluation of Phomopsis amaranthicolasp. nov. as a Biological Control Agent for Amaranthus spp. Ph.D. Dissertation, University of Florida, Gainesville, FL, USA; 1997.
Rosskopf EN, Charudattan R, Shabana YM, Benny GL. Phomopsis amaranthicola. a new species from Amaranthussp. Mycologia 2000;92(1) 114–122.
Rosskopf EN, Charudattan R, Devalerio JT, Stall VM. Field Evaluation of Phomopsis amaranthicola, a Biological Control Agent of Amaranthusspp. Plant Disease 2000;84(11) 1225–1230.
Mintz AS, Heiny DK, Weidemann GJ. Factors Influencing the Biocontrol of Tumble Pigweed ( Amaranthus albus) with Aposphaeria amaranthi. Plant Disease 1992;76(3) 267–269.
Heiny DK, Mintz AS, Weidemann GJ. Redisposition of Aposphaeria amaranthiin Microsphaeropsis. Mycotaxon 1992;44(1) 137–154.
Ortiz-Ribbing L, Williams MM. Potential of Phomopsis amaranthicolaand Microsphaeropsis amaranthi, as Bioherbicides for Several Weedy Amaranthusspecies. Crop Protection 2006;25(1) 39–46.
Hetherington SD, Smith HE, Scanes MG, Auld BA. Effects of Some Environmental Conditions on the Effectiveness of Drechslera avenacea(Curtis ex Cooke) Shoem.: A Potential Bioherbicidal Organism for Avena fatuaL. Biological Control 2002;24(2) 103–109.
Peng G, Byer KN, Bailey KL. Pyricularia setariae: A Potential Bioherbicide Agent for Control of Green Foxtail ( Setaria viridis). Weed Science 2004;52(1) 105–114.
Boyette CD, Hoagland RE, Weaver MA. Interaction of a Bioherbicide and Glyphosate for Controlling Hemp Sesbania in Glyphosate-Resistant Soybean. Weed Biology and Management 2008;8(1) 18–24.
Bailey KL, Derby J, Falk S. Evaluation of Phoma macrostomafor Control of Broadleaf Weeds in Turgrass. VI international Bioherbicide Group Workshop, Canberra, Australia; 2003.
Zhou L, Bailey KL, Derby J. Plant Colonization and Environmental Fate of the Biocontrol Fungus Phoma macrostoma. Biological Control 2004;30(3) 634–644.
Kadir JB, Charudattan R, Stall WM, Brecke BJ. Field Efficacy of Dactylaria higginsiias a Bioherbicide for the Control of Purple Nutsedge ( Cyperus rotundus). Weed Technology 2000;14(1) 1–6.
Kadir JB, Charudattan R, Stall WM, Bewick TA. Effect of Dactylaria higginsiion interference of Cyperus rotunduswith L. esculentum. Weed Science 1999;47(6) 682–686.
Morales-Payan JP, Charudattan R, Stall WM, Devalerio J.T. Efficacy of Dactylaria higginsiito Suppress Purple Nutsedge ( Cyperus rotundus) in Pepper ( Capsicum annuum) is Affected by Some Surfactants. Phytopathology 2003;93 (Suppl.):S63 (Abstr.).
Semidey N, Charudattan R, Morales-Payan JP, Devalerio J.T. Response of Cyperus rotundusand Allium cepato Dactylaria higginsiiin Puerto Rico. XVI Congreso Latinoamericano de Malezas y el XXIV Congreso Nacional de la Asociación Mexicana de la Ciencia de la Maleza, Manzanillo, Colima, Mexico; 2003.
Rosskopf EN, Yandoc C, Devalerio JT, Kadir JB, Charudattan R. Evaluation of the Bioherbicidal Fungus Dactylaria higginsiias a Component of an IPM Approach to Pest Management in Tomato. Phytopathology 2003; 93(6) (Suppl.):S75 (Abstr.).
Mason PG, Huber JT. Biological Control Programmes in Canada 1981-2000. CABI Publishing, Wallingford, Oxon, UK; 2002.
Boyetchko SM. Biological Herbicides in the Future. In: Ivany JA., ed. Weed Management in Transition. Topics in Canadian Weed Science (Vol. 2). Sainte-Anne-de-Bellevue, Quebec. Canadian Weed Science Society - Societe Canadienne de Malherbologie; 2005. p29–47.
Boyetchko SM, Rosskopf EN. Strategies for Developing Bioherbicides for Sustainable Weed Management. In: Singh HP., Batish DR., Kohli RK., eds. Handbook of Sustainable Weed Management. The Haworth Press Inc., Binghamton, NY; 2006. p393–430.
Charudattan R, Elliot M, Devalerio JT, Hiebert E, Pettersen ME. Tobacco Mild Green Mosaic Virus: A Virus-Based Bioherbicide. VI international Bioherbicide Group Workshop, Canberra, Australia; 2003.
Caulder JD, Stowell L. Synergistic Herbicidal Compositions Comprising Colletotrichum truncatumand Chemical Herbicides. US patent 4,775,405. 6 Jan. 1987.
Christy AL, Herbst KA, Kostka SJ, Mullen JP, Carlson SJ. Synergizing Weed Biocontrol Agents with Chemical Herbicides. In: Duke SO., Menn JJ., Plimmer J.R., eds. Pest Control with Enhanced Environmental Safety. American Chemical Society, Washington, DC; 1993. p87–100.
Hoagland RE. Chemical Interactions with Bioherbicides to Improve Efficacy. Weed Technology 1996;10(3) 651–674.
Hoagland RE. Plant Pathogens and Microbial Products as Agents for Biological Weed Control. In: Tewari JP., Lakhanpal TN., Singh J., Gupta R., Chamola V.P., eds. Advances in Microbial Biotechnology. APH Publishing, New Delhi, India; 2000. p213–255.
Caulder JD, Stowell L. Synergistic Herbicidal Compositions Comprising Alternaria cassiaeand Chemical Herbicides. US Patent 4,776,873. 27 Jan. 1987.
Sharon A, Ghirlando R, Gressel J. Isolation, Purification, and Identification of 2-( p-hydroxyphenoxy)-5,6-dihydroxychromone: A Fungal Induced Phytoalexin. Plant Physiology 1992;98(1) 303–308.
Boyette CD, Reddy KN, Hoagland RE. Glyphosate and Bioherbicide Interaction for Controlling Kudzu ( Pueraria lobata), Redvine ( Brunnichia ovata), and Trumpetcreeper ( Campsis radicans). Biocontrol Science and Technology 2006; 6(10) 1067–1077.
Heiny DK. Field Survival of Phoma proboscisand Synergism with Herbicides for Control of Field Bindweed. Plant Diseases 1994;78(12) 1156–1164.
Auld BA. Vegetable Oil Suspension Emulsions Reduce Dew Dependence of a Mycoherbicide. Crop Protection 1993;12(6) 477–479.
Boyette CD. Unrefined Corn Oil Improves the Mycoherbicidal Activity of Colletotrichum truncatumfor Hemp Sesbania ( Sesbania exaltata) Control. Weed Technology 1994;8(3) 526–529.
Egley GH, Boyette CD. Water-Corn Oil Emulsion Enhances Conidia Germination and Mycoherbicidal Activity of Colletotrichum truncatum. Weed Science 1995;43(2) 312–317.
Ghorbani R, Seel W, Litterick A, Leifert C. Evaluation of Alternaria alternatafor Biological Control of Amaranthus retroflexus. Weed Science 2000;48(4) 474–480.
Sandrin TR, TeBeest DO, Weidemann GJ. Soybean and Sunflower Oils Increase the Infectivity of Colleototrichum gloeosporioidesf. sp. aeschynomeneto Northern Jointvetch. Biological Control 2003;26(3) 244–252.
Quimby PCJr, Fulgham FE, Boyette CD, Connick WJJr. An Invert Emulsion Replaces Dew in Biocontrol of Sicklepod - A Preliminary Study. In: Hovde DA., Beestman GB., eds. Pesticide Formulations and Application Systems. ASTM-STP 980. West Conshohocken, PA: American Society for Testing Materials; 1989. p264–270.
Amsellem Z, Sharon A, Gressel J. Abolition of Selectivity of Two Mycoherbicidal Organisms and Enhanced Virulence of Avirulent Fungi by an Invert Emulsion. Phytopathology 1991;81(9) 925–929.
Yang S, Dowler WM, Schaad NW, Connick WJJr. Method for the Control of Weeds with Weakly Virulent or Non-Virulent Plant Pathogens. US Patent No. 5,795,845. 1998.
Makowski RMD. Foliar Pathogens in Weed Biocontrol: Ecological and Regulatory Constraints. In: Andow, DA., Ragsdale DW., Nyvall., RF., eds.Ecological Interactions and Biological Control. Westview Press, Boulder; 1996.
Mortensen K. Constraints in Development and Commercialization of a Plant Pathogen, Colletotrichum gloeosporioidesf. Sp. Malvae,For Biological Weed control. In: Brown H., Cussans G., Devine M., Duke S., Fernandez-Quintanilla C., Helweg A., Labrada R., Landes M., Kudsk P., Streibig J., eds. Proc. 2nd Int. Weed Control Congress. Weed Control, Pesticides, Ecology, Flakkebjerg, Denmark; 1996. p1297–1300.
Kenerley CM, Andrews JH. Interactions of Pathogens on Plant Leaf Surfaces. In: Hoagland RE, ed. Microbes and Microbial Products as Herbicides, ACS Symp. Ser. 439. American Chemical Society, Washington, DC.; 1990. p192–217.
Andrews JH. Biological Control in the Phyllosphere. Annual Review of Phytopathology 1992; 30: 603–635.
Boyette CD, Walker HL. Factors Influencing Biocontrol of Velvetleaf ( Abutilont theophrasti) and Prickly Sida ( Sida spinosa) with Fusarium lateritium. Weed Science 1985;33(2) 209–211.
Wymore LA, Poirier C, Watson AK, Gotlieb AR. Colletotrichum coccodes, a Potential Bioherbicide for Control of Velvetleaf ( Abutilon theophrasti). Plant Disease 1988;72(6) 534–538.
Morin L, Watson AK, Reeleder RD. Effect of Dew, Inoculum Density, and Spray Additives on Infection of Field Bindweed by Phomopsis convolvulus. Canadian Journal of Plant Pathology 1990;12(1) 48–56.
Makowski RMD. Effect of Inoculum Concentration, Temperature, Dew Period, and Plant Growth Stage on Disease of Round-Leaved Mallow and Velvetleaf by Colletotrichum gloeosporioidesf.sp. malvae. Phytopathology 1993; 83(11) 1229–1234.
TeBeest DO, Yang XB, Cisar CR. The Status of Biological Control of Weeds with Fungal Pathogens. Annual Review of Phytopathology 1992;30 637–657.
Auld BA, Say MM, Ridings HI, Andrews J. Field Applications of Colletotrichum orbiculareto Control Xanthium spinosum. Agriculture, Ecosystems and Environment 1990;32(3-4) 315–323.
McRae CF, Auld BA. The Influence of Environmental Factors on Anthracnose of Xanthium spinosum. Phytopathology 1988;78(9) 1182–1186.
Jackson MA, Bothast RJ. Carbon Concentration and Carbon to Nitrogen Ratio Influence Submerged Culture Conidiation by the Potential Bioherbicide Colletotrichum truncatumNRRL 13757. Applied and Environmental Microbiology 1990;56 3435–3438.
Jackson MA, Slininger PJ. Submerged Culture Conidial Germination and Conidiation of the Bioherbicide Colletotrichum truncatumare Influenced by the Amino Acid Composition of the Medium. Journal of Industrial Microbiology and Biotechnology 1993;12(6) 471–482.
Schisler DA, Jackson MA, Bothast RJ. Influence of Nutrition During Conidiation of Colletotrichum truncatumon Conidial Germination and Efficacy in Inciting Disease on Sesbania exaltata.Phytopathology 1991;81(4) 587–590.
Boyette CD, Quimby PCJr, Connick WJJr, Daigle DJ, Fulgham FE. Progress in the Production, Formulation and Application of Mycoherbicides. In: TeBeest DO., ed. Microbial Control of Weeds. Chapman and Hall Inc., New York, NY; 1991. p209–224.
Weidemann GJ. Effects of Nutritional Amendments on Conidial Production of Fusarium solanif. sp. Cucurbitaeon Sodium Alginate Granules and on Control of Texas Gourd. Plant Disease 1988;72(9) 757–759.
Jones RW, Hancock JG. Soilbome Fungi for Biological Control of Weeds. In: Hoagland RE., ed. Microbes and Microbial Products as Herbicides, ACS Symp. Ser. 439. American Chemical Society, Washington, DC; 1990. p276–286.
Charudattan R, Devalerio JT, Prange, VJ. Special Problems Associated with Aquatic Weed Control. In: Baker RR., Dunn, PE., eds. New Directions In Biological Control: Alternatives for Suppressing Agricultural Pests and Diseases. Alan R. Liss Inc., New York, NY; 1990. p287–303.
Gabriel DW. Parasitism, Host Species Specificity, and Gene-Specific Host Cell Death. In: TeBeest DO., ed. Microbial Control of Weeds. Chapman and Hall. New York, NY; 1991. p115–131.
Leonard KJ. The Benefits and Potential Hazards of Genetic Heterogeneity in Plant Pathogens. In: Charudattan R., Walker HL., eds. Biological Control of Weeds with Plant Pathogens. J. Wiley. New York, NY; 1982. p99–112.
Burdon JJ. Diseases and Plant Population Biology. Cambridge University Press, Cambridge, UK; 1987. p208.
Weidemann GJ. TeBeest DO. Genetic Variability of Fungal Pathogens and Their Weed Hosts. In: Hoagland RE., ed. Microbes and Microbial Products as Herbicides, ACS Symp. Ser. 439. American Chemical Society, Washington, DC.; 1990. p176–183.
Nikandrow A, Weidemann GJ, Auld BA. Incidence and Pathogenicity of Colletotrichum orbiculareand a Phomopsissp. on Xanthiumsp. Plant Disease 1990;74(10) 796–799.
Auld BA, Talbot HE, Radburn KB. Host Range of Three Isolates of Alternaria zinniae, a Potential Biocontrol Agent for Xanthiumsp. Plant Protection Quarterly 1992;7(3) 114–116.
De Jong MD, Scheepens PC, Zadoks JC. Risk Analysis for Biological Control: A Dutch Case Study in Biocontrol of Prunus serotinaby the Fungus Chondrostereum purpureum. Plant Disease 1990;74(3) 189–194.
TeBeest DO, Cisar CR, Spiegel FW. Partial Characterization of Progeny from a Cross Between Colletotrichum gloeosporioidesf. sp. aeschynomeneand C. gloeosporioidesfrom Carya. Plant Protection Quarterly 1992;7(4) 171.
Weidemann GJ. Risk Assessment: Determining Genetic Relatedness and Potential Asexual Gene Exchange in Biocontrol Fungi. Plant Protection Quarterly 1992;7(4) 166–168.
Hebbar KP, Lumsden RD, Lewis JA, Poch SM, Bailey BA. Formulation of Mycoherbicidal Strain of Fusarium oxysporum. Weed Science 1998;46(4) 501–507.
Patzoldt WL, Tranel PJ, Alexander AL, Schmizer PR. A common ragweed population resistant to cloransulam-methyl. Weed Science 2001;49(4) 485–490.
Bayer KN, Wolf TM, Caldwell BC, Baiely KL. Assays for Predicting Mycoherbicide Formulation Compatibility. In: Spencer N., Noweierski R., eds. Abstracts of the 10th International Symposium on Biological Control of Weeds. Montana State University, Bozeman, MT, USA, 4–9 July 1999.
Boyette CD, Jackson MA, Quimby PCJr, Connick WJJr, Zidak NK, Abbas HK. Biological Control of the Weed Hemp Sesbania with Colletotrichum truncatum. In: Spencer N., Noweierski R., eds. Abstracts of the 10th International Symposium on Biological Control of Weeds. Montana State University, Bozeman, MT, USA, 4–9 July 1999.
Watson AK, Wymore X. Identifying Limiting Factors in the Biocontrol of Weeds. In: Baker RR., Dunn PE., eds. New Direction in Biological Control: Alternatives for Suppressing Agricultural Pests and Diseases (ed. by). Alan R. Liss, New York, NY; 1990. p305–316.
Daigle DJ, Connick WJ. Formulation and Application Technology for Microbial Weed Control. In: Hoagland RE., ed. Microbes and Microbial Products as Herbicides, ACS Symp. Ser. 439. American Chem. Soc., Washington, DC; 1990. p 288–304.
Womack JG, Burge MN. Mycoherbicide Formulation and the Potential for Bracken Control. Pesticide Science 1993;37(4) 337–341.
Amsellem Z, Sharon A, Gressel J, Quimby PC Jr. Complete Abolition of High Inoculum Threshold of Two Mycoherbicides ( Alternaria cassiaeand A. crassa) When Applied in Invert Emulsion. Phytopathology 1990;80(10) 925–929.
Yang SM, Johnson DR, Dowler WM, Connick WJJr. Infection of Leafy Spurge by Alternaria alternataand A. angustiovoideain the Absence of Dew. Phytopathology 1993;83(9) 953–958.
Connick WJJr, Boyette CD. Host Range and Virulence of Colletotrichum truncatum, a Potential Mycoherbicide for Hemp Sesbania ( Sesbania exaltata). Plant Disease 1991;75(1) 62–64.
Womack JG, Eccleston GM, Burge MN. A Vegetable Oil Based Invert Emulsion for Mycoherbicide Delivery. Biological Control 1996;6(1) 23–28.
Chittick AT, Ash GJ, Kennedy RA, Harper JDI. Microencapsulation: An Answer to the Formulation Quandary? VI international Bioherbicide Group Workshop, Canberra, Australia; 2003.
Gracia-Garza JA, Fravel DR, Bailey BA, Hebbar PK. Dispersal of Formulations of Fusarium oxysporumf. sp. erythroxyliand F. oxysporumf. sp. melonisby Ants. Phytopathology 1998;88(3) 185–189.
Shabana YM, Baka ZA, Abdel-Fattah GM. Alternaria eichhorniae, a Biological Control Agent for Waterhyacinth: Mycoherbicidal Formulation and Physiological and Ultrastructural Host Responses. European Journal of Plant Pathology 1997;103(2) 99–111.
Chittick AT, Auld BA. Polymers in Bioherbicide Formulation: Xanthium spinosumand Colletotrichumas a Model System. Biocontrol Science and Technology 2001;11(6) 691–702.
Klein TA, Auld BA, Fang W. Evaluation of Oil Suspension Emulsions of Colletotrichum orbiculareas a Mycoherbicide in Field Trials. Crop Protection 1995; 14(3) 193–197.
Auld BA. Bioherbicidal Formulations. Australian Provisional Patent Application 2002952094. Patent Office, IP Australia, Canberra; 2002.
Marti-Mestres G, Niellond F. Emulsions in Health Care Applications – An Overview. Journal of Dispersion Science and Technology 2002;23(1-3) 419–439.
De Luca M, Grossoird JL, Medard JM, Vaution C. A Stable W/O/W Multiple Emulsion. Cosmetics Toiletries 1990;105: 65–69.
Cindio B, Grasso G, Cacace D. Water-in-Oil-in Water Double Emulsions for Food Applications: Yield Analysis and Rheological Properties. Food Hydrocolloids 1991;4(5) 339–353.
Pilgeram AL, Carsten LD, Sands DC. Genetic Improvement of Bioherbicides. In: Osiewacz AD., ed. The Mycota, X Industrial Applications. Springer-Verlag, Berlin, Germany; 2002. p367–374.
Ghosheh HZ. Constraints in Implementing Biological Weed Control: A Review. Weed Biology and Management 2005;5(3) 83–92.