Abstract
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.
Keywords
- Bioherbicide (inundative) approach
- advantages
- restrictions
1. Introduction
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 [4]. 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 [10], and not as a replacement for chemical herbicides and other weed management tactics [11]. 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 [12].
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
effectiveness for managing herbicide-resistant (HR) weed populations [7,9,12–16].
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) [17];
environment restrictions (epidemiology of bioherbicides reliant on optimal environmental conditions) [18–20];
technical restrictions (wholesale production and formulation development of reliable and effective bioherbicide) [17,21]; and
commercial restrictions (market capacity, patent protection, confidence and adjustment) [21–23].
2. Biological weed control
Biological control is the deliberate use of natural enemies to reduce the population of a target weed to below a desired threshold [24,25] and can be divided into two main approaches:
classical approach, in which a natural enemy is exported from its native range to an introduced (weedy, invasive) range of a plant, [24,26,27], and
bioherbicide approach, in which a natural enemy is used within its native range to control a native or naturalized weed [28–30].
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 [31]. 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 [32]. 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 (
Trujillo
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 [28]. These are utilized at amounts that will provoke tremendous levels of infection, leading to elimination of the target weed before economic damages happen [29]. 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 [30]. 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 [109], 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 [21]. 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 [115]. 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. [113] reported for 95% control of the emerging
There are many environmental limitations to applying bioherbicides and maintaining their efficacy in water as well [118]. Auld and McRae [4] 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 [8] 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 [17]. In other words, within a population of weed species there will usually be a range of genetically diverse biotypes [121] that may include some resistant biotypes, just as there may be a range of biotypes of microorganisms [122], 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 [21]. 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 [129]. 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 [130].
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 [132] 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 [135], 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 [135]. Invert emulsions consist of a continuous oil phase that contains water droplets. Connick and Boyette [137] have developed an invert emulsion formulation exhibiting lower viscosity and greater water-retention properties. Auld [93] 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 [139]. 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 [140].
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 [110]. Pathogenicity of an aqueous mycelial inoculum of
A novel bioherbicide formulation uses a complex emulsion – water-in-oil-in-water (WOW) emulsion [144]. It contains at least one lipophilic surfactant, at least one hydrophilic surfactant, oil and water. Although used in the pharmaceutical [145], cosmetic [146] and food industries [147], 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 [148].
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 [149]. 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].
10. Conclusion
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.
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