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Review

Towards Sustainable Green Adjuvants for Microbial Pesticides: Recent Progress, Upcoming Challenges, and Future Perspectives

State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops & Key Laboratory of Biopesticide and Chemical Biology of Ministry of Education & Biopesticide Research Center, College of Life Sciences & College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou 350002, China
*
Author to whom correspondence should be addressed.
Microorganisms 2023, 11(2), 364; https://doi.org/10.3390/microorganisms11020364
Submission received: 28 December 2022 / Revised: 28 January 2023 / Accepted: 29 January 2023 / Published: 31 January 2023
(This article belongs to the Special Issue Biological Control of the Plant Pathogens)

Abstract

:
Microbial pesticides can be significantly improved by adjuvants. At present, microbial pesticide formulations are mainly wettable powders and suspension concentrations, which are usually produced with adjuvants such as surfactants, carriers, protective agents, and nutritional adjuvants. Surfactants can improve the tension between liquid pesticides and crop surfaces, resulting in stronger permeability and wettability of the formulations. Carriers are inert components of loaded or diluted pesticides, which can control the release of active components at appropriate times. Protective agents are able to help microorganisms to resist in adverse environments. Nutritional adjuvants are used to provide nutrients for microorganisms in microbial pesticides. Most of the adjuvants used in microbial pesticides still refer to those of chemical pesticides. However, some adjuvants may have harmful effects on non-target organisms and ecological environments. Herein, in order to promote research and improvement of microbial pesticides, the types of microbial pesticide formulations were briefly reviewed, and research progress of adjuvants and their applications in microbial pesticides were highlighted, the challenges and the future perspectives towards sustainable green adjuvants of microbial pesticides were also discussed in this review.

1. Introduction

In modern agriculture and forestry, pesticides have always played important roles in ensuring agricultural production as a necessity to increase grain production, regulate crop growth, and control plant pests and diseases [1,2]. Following economic globalization, the problems of chemical pesticide residue have attracted the attention of many countries. Many of them have increasingly strict trade standards for pesticide residue in agricultural products. Ideally, pesticides must be lethal to target pests, but not to non-target species, including humans [1,3,4]. Microbial pesticides, mainly produced with naturally occurring bacteria, fungi (including some protozoa and yeasts), and viruses, have been attracting widespread attention due to their advantages in target specificity, environmental safety, efficacy, biodegradability, and applicability in integrated pest management programs [5,6,7].
The United States is the first country in the world to manage pesticide additives. In 1954, the United States FDA implemented the ADI limit. In 1987, according to the policy of “Reducing the potential adverse effects of the use of pesticide products containing toxic inert ingredients”, the United States EPA conducted classified list management on the toxicity and exposure hazards of additives (divided into four categories) [8,9]. The European Union, through the implementation of REACH system, divides pesticide additives into three categories of management, requiring that the limits of 227 substances with potential risks among more than 3200 agricultural chemicals should be marked on the labels, and has clearly stipulated that benzene organic solvents, nonylphenol/octylphenol polyoxyethylene ether, and bovine ester amine surfactants should be restricted or prohibited in pesticide preparations [10]. At present, China has not implemented systematic management of pesticide adjuvants, But a series of regulations have been put in place to regulate some adjuvants [11].
Commercial pesticide preparations are always a mixture of “active ingredients” and “other ingredients” (adjuvants) [12,13]. Biocontrol agents are formulations produced from living organisms or substances produced by them for the control of pests or diseases. Biopesticides are formulations that use living organisms (fungi, bacteria, insect viruses, genetically modified organisms, natural enemies, etc.) or their metabolites (pheromones and auxin, etc.) to kill or inhibit agricultural pests [14,15]. The proportion of bacteria as the main active ingredient of microbial pesticides is the largest, followed by fungi, viruses, and genetically modified microorganisms. Bacillus thuringiensis (Bt) bacterial insecticide is the most widely used and most productive microbial insecticide in the world, accounting for 95% of microbial insecticides [16,17,18].
Since the active ingredients of microbial pesticides are mainly microorganisms and their bioactive compounds, their growth and reproduction in the field are affected by environmental factors such as temperature, humidity, and ultra-violet (UV) ray radiation [19]. The microorganisms have strong hydrophobicity and are likely to form large particles in solutions, which make the pesticides difficult to use to solve field application problems such as wettability and suspension [20]. The drawbacks may be overcome by the application of adjuvants to deliver the active ingredients to targets because adjuvants can effectively improve physical and chemical properties of pesticide preparations. There are more than three thousand kinds of pesticide adjuvants in common use. The value of pesticide adjuvants market in 2015 was USD 2.51 billion [19]. To date, adjuvants are developing towards multi-function adjuvants with characteristics that make them labor-saving, low consumption, easy degradation, and low toxicity. They are often applied as wetting agents and emulsifiers in the production of pesticide formulations [21,22].
Green pesticide is harmless to human health, friendly to the environment, ultra-low dosage, high selectivity, and through the green process to produce pesticides [23]. At present, most of the adjuvants used in microbial pesticides still refer to those of chemical pesticides [24]. A green adjuvant is a kind of non-toxic, harmless, and good biodegradable adjuvant added in the process of pesticide production [25]. Biogenic adjuvants are traditionally green, but adjuvants synthesized from fine chemicals are also partially green. Some traditional adjuvants are mostly chemical adjuvants, which have different effects on the active ingredients and the environment. Compared with green adjuvants, it can improve the performance of the preparation and has no impact on the environment. With the development of green agriculture, the safety of pesticides and green pesticide adjuvants is particularly important. [26,27,28]. Herein, in order to promote the research and development of better microbial pesticides, types of microbial pesticide formulations were briefly reviewed, and research progress of adjuvants and their applications in microbial pesticides were highlighted, while the challenges and the future perspectives towards sustainable green adjuvants of microbial pesticides were also discussed.

2. Types of Microbial Pesticide Formulations

There are many formulations of microbial pesticides such as wettable powders, suspensions, oil suspensions, water dispersible granules, and suspension seed coatings (Table 1) [29,30,31]. However, the production of microbial pesticides is relatively more complicated than those of chemical pesticides [32,33]. During the preparation process, the microorganisms in the pesticides are more sensitive to external environmental factors such as UV rays, temperature, and humidity [34]. Compared with chemical pesticides, relatively slow action affects the application efficiency of microbial pesticides. The microorganisms, which are mainly bacteria, fungi, or viruses, are insoluble biological particulate matters from 0.5 μm to 1000 μm. They will directly affect the physical properties of the pesticide preparations such as suspension, dispersibility, and wettability [35].

3. Classifications and Functions of Adjuvants Used for Microbial Pesticides

The adjuvants used in the production of microbial pesticides are mainly classified into four categories: surfactants, carriers, protective agents, and nutritional adjuvants.

3.1. Surfactants

Surfactants can improve cost-effectiveness, increase processing efficiency, and save energy and raw materials for the production of microbial pesticides (Figure 1). They play important roles in maintaining long-term physical stability and improving biological functions of the pesticides [36]. About 3.4 million tons of surfactants were produced in 2019, and microbial pesticides usually contain one or more surfactants [37,38].
Surfactants have special molecular structures (amphiphilic structures) consisting of hydrophobic and hydrophilic groups [39,40]. They can be divided into cationic, anionic, nonionic, and amphoteric types by their hydrophilic groups (Table 2 and Figure 2) [41]:
(1)
Cationic surfactants: The hydrophilic part is mainly quaternary ammonium ions with strong antibacterial properties [36];
(2)
Anionic surfactants: They mainly include ionic sulfonates, sulfates, and carboxylate, most of which contain sodium or calcium. Straight chain alkyl sulfonates occupy the largest market share of all anionic surfactants [42];
(3)
Nonionic surfactants: They have polymerized glycol ether and glucose units, which are mainly used as emulsifiers and wetting agents [43,44];
(4)
Amphoteric surfactants: Contain both cationic and anionic groups in their structures. They are not only soluble in water, but also highly compatible with other surfactants to form mixed micelles. Their electric charges vary with pH, thereby affecting pesticide properties such as wetting, sedation, and foaming [36].
Table 2. Main surfactants used for the production of microbial pesticides.
Table 2. Main surfactants used for the production of microbial pesticides.
TypesMain ProductsFeaturesReferences
Cationic surfactantsStearyl trimethyl ammonium chloride (STAC) and Hexadecyl trimethyl ammonium bromide (TTAB)Good water solubility, strong bactericidal power, and adsorption power; cannot be used with anionic surfactants[45]
Anionic surfactantsCalcium dodecylben-zenesulfonate (ABSCa) and Sodium 2-butyl-1-naphthalenesulfonate (BX)Good solubility, safety and low toxicity, and strong stability[46]
Nonionic surfactantsDibenzyl biphenyl polyoxyethylene ether, Defoamer GP330 and tween-80Good environmental adaptability, strong stability; cannot be affected by strong electrolytes, acids, and bases[47]
Amphoteric surfactantsDodecyl dimethyl betaine (BS-12)High cost with strong permeability, flocculation, adhesion, resistance reduction, and thickening[48]

3.2. Carriers

The main function of a carrier is to act as a tiny container or diluent for active ingredients of microbial pesticides [20]. The mass percentage of a carrier may exceed that of the active ingredient in the pesticide [49,50]. Carriers such as diatomite, attapulgite, silica, and bentonite with strong adsorption capacities can be used to manufacture high-concentration powders, wettable powders, or granules (Table 3) [51]. Carriers such as talc, pyrophyllite, sepiolite, and clay materials with low or moderate adsorption capacities are generally used as diluents and fillers to produce low-concentration powders (Table 3) [52]. Their pore structures and specific surface areas enable the pesticides to be released into the environments at relatively slow rates [53,54]. Carriers made with biodegradable materials also enable targeted and controlled release of active ingredients from microbial pesticides [55]. For example, chitosan/carbon nanotube nanocomposites were used as the carrier of controlled-release pesticides and prepared, uniformly dispersed carbon nanotube-enhanced Cs films were applied to reduce the harm of pesticides to the environment during the release process [56,57]. Biodiesel may be used as a dilution carrier in liquid pesticide formulations [58]. Some natural plants and synthetic substances are also commonly used as carriers (Table 3) [59].
In the screening process of microbial pesticide carriers, the biocompatibility of carriers and microorganisms in microbial pesticides is the primary concern [67]. Herein, a typical microbial pesticide formulation will select a carrier with good biocompatibility. And the formulation may also rely on wetting and dispersing agents to further improve its wetting and dispersing properties [68]. However, a suitable carrier can confer enough wettability for microbial pesticide formulations without the help of other adjuvants [69]. In fact, carriers greatly affect the wetting, suspending, and dispersing properties of microbial pesticide formulations [35].

3.3. Protective Agents

They are mainly divided into the following two categories:
(1)
UV protective agents
UV radiation causes passivation, degradation, or damage to microbial pesticides(Figure 2) [70]. UV rays can inhibit the growth of microorganisms, and even cause them to die in severe cases. UV protection agents used for the production of microbial pesticides are mainly divided into UV ray absorbers and anti-oxidative UV protection agents. UV ray absorbers such as locust toxin, optical brighteners, lignosulfonates, and milk can absorb the UV part of sunlight and fluorescent light sources without changing itself [71]. Anti-oxidative UV protection agents such as Rubus oil, hemp seed oil, kojic acid, hydroxykynurenic acid, flavonoids, and lecithin have strong antioxidant effects to help microbial pesticides to avoid being easily oxidized and degraded into other substances that are ineffective against harmful organisms under the irradiation of UV rays. Recently, the development of nanomaterials also provides new ideas for novel UV protective agents [72]. Although UV protective agents such as melanin, berberine, fluorescent whitening agents, and Congo red have significant photoprotective effects on Bt, they are cytotoxic to Bt, and may have a certain impact on the environment [73]. Herein, environmental friendliness should also be considered when UV protective agents are developed.
(2)
Other protective agents
Microorganisms in microbial pesticide preparations are easily affected by adverse factors such as temperature, humidity, and oxidation during storage and transportation, which reduce the viable microorganism rate in the formulations and affect their field control effects. Protective agents may also improve the control effect of microbial pesticides in the field and prolong their shelf lives [74]. For example, a protective agent comprised of 8.00% NaCl and 1.00% sodium acetate can increase the spore survival rate of a Bacillus subtilis preparation by 22.53% [75]. The addition of protective adjuvants depends on the quality of the biomaterial. In addition to benzoic acid or other chemicals, Bacillus spores can be kept for many years without other protective substances to prevent contamination [76].

3.4. Nutritional Adjuvants

During the growth of microorganisms, they need water, inorganic salts, carbon sources, nitrogen sources, and growth factors to grow normally. Nutritional adjuvants can provide nutrients to microorganisms of microbial pesticides to improve their reproductive capacity and promote their proliferation and growth in the field. At present, the research on nutritional adjuvants mainly focuses on the supplementation of carbon and nitrogen sources [77].

4. Application of Adjuvants in Microbial Pesticide Formulations

The majority of microbial pesticide formulations are wettable powders and suspension concentrations. Therefore, this section first introduces the applications of adjuvants in them and takes into account other applications.

4.1. Application of Adjuvants in Wettable Powders of Microbial Pesticides

A wettable powder refers to a pesticide formulation produced with active ingredients and adjuvants such as carriers, wetting agents, stabilizers, and UV protective agents [78]. The average particle size of a wettable powder is about 44 μm with a ≧ 75% suspension rate and a < 2 min wetting time [79,80]. It can form a stable suspension with good dispersibility after being dissolved and stirred in water and is generally used for spraying in the field [81]. Microbial pesticides, comprised of both microorganisms insoluble in water and organic solvents as the active ingredients, are suitable for processing into wettable powders [82]. Transportation and packaging costs of wettable powders are relatively low. The percentage of active ingredients in the pesticides is higher than that of powders and renders good adhesion to the crops after spraying. However, the powders may not be uniformly dispersed and suspended in the solution during the application, causing problems such as blockage of the nozzle and uneven spraying [83]. Half of registered Bt formulations are wettable powders, which play important roles in the formulations of microbial pesticides [78,84].
Carriers are crucial to wettable powders because the first step of the production is to culture microorganisms to obtain fermentation broths. Substances with strong adsorption properties such as silica, bentonite, attapulgite, and diatomite may be selected as carriers, whose effects on the survival states of microorganisms should also be considered [85]. Biocompatibility is the primary consideration to select a microbial pesticide carrier. At present, the primary evaluation method of biocompatibility is to mix carriers with microorganisms to investigate their survival rates [86]. There are some limitations to this approach. When encountering an adverse external environment, microorganisms will enter dormancy or spore state and survive well, and the carriers cannot show incompatibility with them [87].
Wetting agents such as sodium lauryl sulfate, stretch powder, polyethylene glycol, calcium lignosulfonate, sodium carboxymethyl cellulose, sodium dodecylbenzene sulfonate, sodium tripolyphosphate, lignin, and sodium sulfonate can also be added in the formulations to reduce the interfacial tension between liquid and solid to increase the adhesion of liquid to solid surface [88,89]. In the storage and transportation of microbiological pesticides, the influence of a wetting agent on the water activity of microbiological pesticides should be considered. Under certain water activity conditions, the active microorganism can maintain a relatively good storage state [90].
Stabilizers such as sodium carboxymethyl cellulose, potassium dihydrogen phosphate, calcium carbonate, and methyl cellulose are also key adjuvants for wettable powders [91,92]. Taking Bacillus as an example, spores are an important factor to help the bacteria resist adverse environments by protecting the spores from decomposition caused by high temperature [70].
The microorganisms in the pesticides are very sensitive to UV rays in a natural environment. Herein, it is necessary to add UV protective agents to the production of wettable powders [93].

4.2. Application of Adjuvants in Suspension Concentrations of Microbial Pesticides

A suspension concentrate, which is formed with active ingredients, carriers, and other adjuvants, is super-pulverized by a sander wet method. Generally, its melting point is higher than 60 °C, which is similar with the characteristics of both emulsifiable concentrates and wettable powders [94]. Suspension concentrates can be mainly classified into water suspension concentrates, oil suspension concentrates, and dry suspension concentrates. They do not use organic substances as solvents and have no risk of inflammability and explosion [82]. They have low toxicities to humans and animals. They are convenient for storage and transportation and can be better sprayed by aircrafts than wettable powders. When applied in the field, they can be mixed with any proportion of water, and easily to adhere to crop surfaces. The production process of a suspension concentrate is relatively simple and environmentally friendly, making it the mainstream formulation for microbial pesticides [95].
The fermentation broth of microorganisms is directly used for the production of suspension concentrates, which are prone to agglomeration, freezing, and precipitation due to the fluidity of the fermentation broth. Herein, adjuvants such as preservatives, dispersants, and stabilizers may be included in the formulations. Preservatives such as potassium sorbate, ethyl p-hydroxybenzoate, and sodium benzoate need to have a good inhibitory effect on mold, yeast, and aerobic bacteria in order to store the suspension concentrations for a long time [96]. The particles of microbial pesticides can automatically aggregate in the solvent, making the surface free energy of the formulations decrease, thereby forming thermodynamically stable systems. A dispersant can make the pesticide particles become smaller, preventing the particles from sedimentation and agglomeration. Dispersants such as calcium lignosulfonate and carboxymethyl cellulose play important roles in maintaining the formulation stability [97]. Stabilizers such as xanthogen glue and magnesium aluminum silicate can control the sizes of the formulation droplets and prevent them from drifting during spraying [98].

4.3. Application of Adjuvants in Other Formulations of Microbial Pesticides

Besides the above two formulations, granules, water-dispersible granules, and suspended seed coatings are also often applied in the production of microbial pesticides [99].
Granules are solid and granulated with active ingredients and adjuvants. Their diameter is 300–1700 microns. Their application is convenient, and their absorption and dissolution efficiency are fast. Compared with wettable powders and suspension concentrates, the granules need adjuvants such as binders, colorants, lubricants, and disintegrating agents [75]. Binders, connecting same or different solid materials, are hydrophilic or hydrophobic and indispensable to the formulation. Colorants have functions of warning and classification for microbial pesticides. Lubricants are used to reduce the excessive pressure in the manufacturing process of granules. Disintegrating agents such as NaCl, AlCl3, and CaCl2 are applied to accelerate the disintegration rates of the granules [100].
Water-dispersible granules are granular formulations that can be rapidly disintegrated and dispersed into a suspension after adding water. Dispersants, binders, and disintegrating agents are indispensable for accelerating their disintegration rate in water [101]. They also need wetting agents, anti-caking agents, and defoamers. The wetting agents are intended to increase the wetting rates of pesticide particles into water and to improve the penetration of water into the granules [102]. Anti-caking agents such as silica gel prevent the formulation from caking by acting as a layer of sliding balls [99].
Suspension seed coatings are flowable and stable uniform suspensions made with active ingredients, adjuvants, and water by wet grinding. The production process is simple and the coating efficiency is high. However, they also have some disadvantages, including aggregation of pesticide particles rendered by long-term storage, and poor coating caused by sedimentation [103]. The formulation needs wetting agents such as alkyl sulfate, lignin sulfur salt, and fatty amine polyoxyethylene ether to reduce the surface tension of solid-liquid interfaces. Xanthan gum can be used to adjust the viscosity of the formulation [104]. Film-forming agents are indispensable to the formulation in that they can bond together and evenly wrap around the outside of the seeds. They are polymer composite materials such as PVA series, PEG macromolecule series, and gum arabic with good air permeability and water permeability. Colorants such as rhododendron in red are also applied to prevent from misuse during storage [105].

5. Challenges towards Sustainable Green Adjuvants for Microbial Pesticides

At present, the adjuvants of microbial pesticides are facing many challenges. The author summarizes the following points:
First of all, adjuvants of microbial pesticides are commonly considered to be inert adjuvants without activities. However, some adjuvants may be toxic to non-target organisms and environment [19]. For example, the U.S. Environmental Agency has conducted toxicity analyses on more than 2000 kinds of adjuvants, of which 26% are mutagenic, teratogenic, and carcinogenic (triple effects). They may also have neurotoxicity, endocrine disrupting effects, and cause harmful reproductive damage [59,106].
Secondly, wettable powder formulations of microbial pesticides on the market are very popular with the help of adjuvants [91,107]. However, their particles are relatively coarse, which is not conducive to coverage of crop surfaces, and absorption and utilization of crops.
Finally, the production process of suspension concentrations is relatively simple and cost-effective, but the liquid formulations are not conducive to the storage of microorganisms compared with wettable powders. Drawbacks such as layering, creaming, crystallization, heat storage solidification, room temperature thickening, and short shelf life also need to be solved during the development of suspension concentrations [71,108].

6. Future Perspectives

The concept of green pesticides has been gradually accepted by the pesticide industry; consequently, they are actively promoting the use of more environmentally friendly solvents and substances [12,109]. Compared to chemical pesticides, desirable properties of microbial pesticides include target specificity, low environmental persistence, and low non-target biological toxicities [110].
At present, most microbial pesticide adjuvants are very similar to those of chemical pesticides [111]. It is necessary to establish standard administration systems for various adjuvants used for microbial pesticides. That is, all adjuvants of microbial pesticides should be subject to the same risk assessments as that of the active ingredients.
Since the active ingredients of microbial pesticides are microorganisms, the effects of adjuvants on the survival and proliferation of the microorganisms should be considered [59]. That is, biocompatibility between the adjuvants and microorganisms used for microbial pesticides should be determined in storage periods. The effects of adjuvants on the proliferation of microorganisms in crop fields should also be investigated after the application of microbial pesticides.
Focus should also be placed on ensuring adjuvants have stronger adsorption capacity, higher dispersion performance, and better safety in order to enhance biocontrol efficiency of microbial pesticides by improving physical and chemical properties of adjuvants.
Microbial pesticides are key products for the development of sustainable and efficient green agriculture [112]. They will replace highly toxic and highly residual chemical pesticides with the help of sustainable green adjuvants.

Author Contributions

Conceptualization, F.L., Y.M., A.L.I. and T.H.; writing—original draft preparation, F.L.; literature searching, F.L., Q.L. and Y.M.; figure preparation, F.L., S.Z. and F.Z.; writing—review and editing, all authors; supervision, T.H.; funding acquisition, X.G. and T.H. All authors have read and agreed to the published version of the manuscript.

Funding

This project is supported by the Fujian Science and Technology Planning Project (No. 2020N5014), the Fujian Agriculture and Forestry University Projects (No. KFb22056XA, No. K1520005A03, the First-class Ecology Discipline Project, the “Research Advances in Life Science” Project and the “Special Topics on Bioscience” Project), and the National Natural Science Foundation of China (No. 31672084). The authors sincerely thank the laboratory members for their help.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Aktar, W.; Sengupta, A. Impact of pesticides use in agriculture: Their benefits and hazards. Interdiscip. Toxicol. 2009, 2, 1–12. [Google Scholar] [CrossRef] [Green Version]
  2. Blair, A.; Ritz, B.; Wesseling, C.; Freeman, L.B. Pesticides and human health. Occup. Environ. Med. 2015, 72, 81–82. [Google Scholar] [CrossRef] [PubMed]
  3. Kim, K.H.; Kabir, E.; Jahan, S.A. Exposure to pesticides and the associated human health effects. Sci. Total Environ. 2017, 575, 525–535. [Google Scholar] [CrossRef] [PubMed]
  4. Pan, X.; XU, J.; Liu, X. 2Progress of the discovery, application, and control technologies of chemical pesticides in China. J. Integr. Agric. 2019, 18, 840–853. [Google Scholar] [CrossRef] [Green Version]
  5. Aldas-Vargas, A.; van der Vooren, T.; Rijnaarts, H.H.M.; Sutton, N.B. Biostimulation is a valuable tool to assess pesticide biodegradation capacity of groundwater microorganisms. Chemosphere 2021, 280, 130793. [Google Scholar] [CrossRef] [PubMed]
  6. Arthurs, S.; Dara, S.K. Microbial biopesticides for invertebrate pests and their markets in the United States. J. Invertebr. Pathol. 2019, 165, 13–21. [Google Scholar] [CrossRef]
  7. Kumar, S.; Singh, A. Biopesticides: Present Status and the Future Prospects. J. Fertil. Pestic. 2015, 6, e129. [Google Scholar] [CrossRef]
  8. Cox, C.; Surgan, M. Unidentified inert ingredients in pesticides: Implications for human and environmental health. Environ. Health Perspect. 2006, 114, 1803–1806. [Google Scholar] [CrossRef] [Green Version]
  9. Mohammad, N.; Abidin, E.Z.; How, V.; Praveena, S.M.; Hashim, Z. Pesticide management approach towards protecting the safety and health of farmers in Southeast Asia. Rev. Environ. Health 2018, 33, 123–134. [Google Scholar] [CrossRef]
  10. Parinya, P.; Siriwong, W.; Prapamontol, T.; Ryan, P.B.; Fiedler, N.; Robson, M.G.; Barr, D.B. Agricultural pesticide management in Thailand: Status and population health risk. Environ. Sci. Policy 2012, 17, 72–81. [Google Scholar]
  11. Wang, T.; Zhong, M.; Lu, M.; Xu, D.; Xue, Y.; Huang, J.; Blaney, L.; Yu, G. Occurrence, spatiotemporal distribution, and risk assessment of current-use pesticides in surface water: A case study near Taihu Lake, China. Sci. Total Environ. 2021, 782, 146826. [Google Scholar] [CrossRef] [PubMed]
  12. Fan, T.; Chen, C.; Fan, T.; Liu, F.; Peng, Q. Novel surface-active ionic liquids used as solubilizers for water-insoluble pesticides. J. Hazard. Mater. 2015, 297, 340–346. [Google Scholar] [CrossRef] [PubMed]
  13. Góngora-Echeverría, V.R.; García-Escalante, R.; Rojas-Herrera, R.; Giácoman-Vallejos, G.; Ponce-Caballero, C. 2020Pesticide bioremediation in liquid media using a microbial consortium and bacteria-pure strains isolated from a biomixture used in agricultural areas. Ecotoxicol. Environ. Saf. 2020, 11, 07–34. [Google Scholar] [CrossRef]
  14. Do Nascimento, J.; Cristina Goncalves, K.; Pinto Dias, N.; Luiz de Oliveira, J.; Bravo, A.; Antonio Polanczyk, R. Adoption of Bacillus thuringiensis-based biopesticides in agricultural systems and new approaches to improve their use in Brazil. Biol. Control 2022, 165, 104792. [Google Scholar] [CrossRef]
  15. Dwivedi, S.A.; Singh, R.S. Synthetic insecticides and bio-pesticide affect natural enemies of aphid (Lipaphis erysimi kalt) in mustard. Indian J. Agric. Res. 2022, 56, 717–725. [Google Scholar] [CrossRef]
  16. Bravo, A.; Likitvivatanavong, S.; Gill, S.S.; Soberón, M. Bacillus thuringiensis: A story of a successful bioinsecticide. Insect Biochem. Mol. Biol. 2011, 41, 423–431. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  17. Duke, S.O.; Powles, S.B. Glyphosate: A once-in-a-century herbicide. Pest Manag. Sci. 2008, 63, 1100–1106. [Google Scholar] [CrossRef]
  18. Ramakrishnan, B.; Venkateswarlu, K.; Sethunathan, N.; Megharaj, M. Local applications but global implications: Can pesticides drive microorganisms to develop antimicrobial resistance? Sci. Total Environ. 2019, 654, 177–189. [Google Scholar] [CrossRef]
  19. Mesnage, R.; Antoniou, M.N. Ignoring Adjuvant Toxicity Falsifies the Safety Profile of Commercial Pesticides. Front. Public Health 2018, 45, 361. [Google Scholar] [CrossRef] [Green Version]
  20. Borger, C.P.D.; Riethmuller, G.P.; Ashworth, M.; Minkey, D.; Hashem, A.; Powles, S.B. Increased Carrier Volume Improves Preemergence Control of Rigid Ryegrass (Lolium rigidum) in Zero-Tillage Seeding Systems. Weed Technol. 2013, 27, 649–655. [Google Scholar] [CrossRef]
  21. Gouli, V.V.; Provost, C.; Parker, B.L.; Skinner, M.; Gouli, S.Y. Comparison of two methods for estimation of spray deposits after application of microbial pesticides. Biocontrol Sci. Technol. 2010, 20, 331–337. [Google Scholar] [CrossRef]
  22. Nobels, I.; Spanoghe, P.; Haesaert, G.; Robbens, J.; Blust, R. Toxicity ranking and toxic mode of action evaluation of commonly used agricultural adjuvants on the basis of bacterial gene expression profiles. PLoS ONE 2011, 6, e24139. [Google Scholar] [CrossRef] [Green Version]
  23. Khursheed, A.; Rather, M.A.; Jain, V.; Wani, A.R.; Rasool, S.; Nazir, R.; Malik, N.A.; Majid, S.A. Plant based natural products as potential ecofriendly and safer biopesticides: A comprehensive overview of their advantages over conventional pesticides, limitations and regulatory aspects. Microb. Pathog. 2022, 173 Pt A. [Google Scholar] [CrossRef] [PubMed]
  24. Borges, S.; Alkassab, A.T.; Collison, E.; Hinarejos, S.; Jones, B.; McVey, E.; Roessink, I.; Steeger, T.; Sultan, M.; Wassenberg, J. Overview of the testing and assessment of effects of microbial pesticides on bees: Strengths, challenges and perspectives. Apidologie 2021, 52, 1256–1277. [Google Scholar] [CrossRef] [PubMed]
  25. Beck, B.; Steurbaut, W.; Spanoghe, P. How to define green adjuvants. Pest Manag. Sci. 2012, 68, 1107–1110. [Google Scholar] [CrossRef] [PubMed]
  26. Dechesne, A.; Badawi, N.; Aamand, J.; Smets, B.F. Fine scale spatial variability of microbial pesticide degradation in soil: Scales, controlling factors, and implications. Front. Microbiol. 2014, 5, 667. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  27. Idris, A.L.; Fan, X.; Muhammad, M.H.; Guo, Y.; Guan, X.; Huang, T. Ecologically controlling insect and mite pests of tea plants with microbial pesticides: A review. Arch. Microbiol. 2020, 202, 1275–1284. [Google Scholar] [CrossRef] [PubMed]
  28. Pickard, F.C.; Simmonett, A.C.; Rigoberto Brooks, B. Efficient High Accuracy Non-Bonded Interactions in the CHARMM Simulation Package. Biophys. J. 2015, 108, 159a. [Google Scholar] [CrossRef] [Green Version]
  29. Kumar, K.K.; Sridhar, J.; Murali-Baskaran, R.K.; Senthil-Nathan, S.; Kaushal, P.; Dara, S.K.; Arthurs, S. Microbial biopesticides for insect pest management in India: Current status and future prospects. J. Invertebr. Pathol. 2019, 165, 74–81. [Google Scholar] [CrossRef] [PubMed]
  30. Mnif, I.; Ghribi, D. Potential of bacterial derived biopesticides in pest management. Crop Prot. 2015, 77, 52–64. [Google Scholar] [CrossRef]
  31. Zhu, L.; Wang, Z.; Zhang, S.; Long, X. Fast microencapsulation of chlorpyrifos and bioassay. J. Pestic. Sci. 2010, 35, 339–343. [Google Scholar] [CrossRef] [Green Version]
  32. Jamshidnia, A.; Abdoli, S.; Farrokhi, S.; Sadeghi, R. Efficiency of spinosad, Bacillus thuringiensis and Trichogramma brassicae against the tomato leafminer in greenhouse. BioControl 2018, 63, 619–627. [Google Scholar] [CrossRef]
  33. Vemmer, M.; Patel, A. v. Review of encapsulation methods suitable for microbial biological control agents. Biol. Control 2013, 67, 380–389. [Google Scholar] [CrossRef]
  34. Jalali, E.; Maghsoudi, S.; Noroozian, E. Ultraviolet protection of Bacillus thuringiensis through microencapsulation with Pickering emulsion method. Sci. Rep. 2020, 10, 20633. [Google Scholar] [CrossRef] [PubMed]
  35. Shukla, P.G.; Kalidhass, B.; Shah, A.; Palaskar, D. v. Preparation and characterization of microcapsules of water-soluble pesticide monocrotophos using polyurethane as carrier material. J. Microencapsul. 2002, 19, 293–304. [Google Scholar] [CrossRef] [PubMed]
  36. Castro, M.J.L.; Ojeda, C.; Cirelli, A.F. Advances in surfactants for agrochemicals. Environ. Chem. Lett. 2014, 12, 85–95. [Google Scholar] [CrossRef]
  37. Edser, C. Multifaceted role for surfactants in agrochemicals. Focus Surfactants 2007, 3, 1–2. [Google Scholar] [CrossRef]
  38. Hernández-Soriano, M.C.; Mingorance, M.D.; Peña, A. Interaction of pesticides with a surfactant-modified soil interface: Effect of soil properties. Colloids Surf. A Physicochem. Eng. Asp. 2007, 306, 49–55. [Google Scholar] [CrossRef]
  39. Janků, J.; Bartovská, L.; Soukup, J.; Jursík, M.; Hamouzová, K. Densitysity and surface tension of aqueous solutions of adjuvants used for tank-mixes with pesticides. Plant Soil Environ. 2012, 58, 568–572. [Google Scholar] [CrossRef] [Green Version]
  40. Krogh, K.A.; Halling-Sørensen, B.; Mogensen, B.B.; Vejrup, K. v. Environmental properties and effects of nonionic surfactant adjuvants in pesticides: A review. Chemosphere 2003, 50, 871–901. [Google Scholar] [CrossRef]
  41. Farming, O. CO and Ni: A Review. Media 2009, 136, 2–13. [Google Scholar] [CrossRef]
  42. Zhao, X.; Chen, Z.; Yu, L.; Hu, D.; Song, B. Investigating the antifungal activity and mechanism of a microbial pesticide Shenqinmycin against Phoma Sp. Pestic. Biochem. Physiol. 2018, 147, 46–50. [Google Scholar] [CrossRef] [PubMed]
  43. Mascarin, G.M.; Jaronski, S.T. The production and uses of Beauveria bassiana as a microbial insecticide. World J. Microbiol. Biotechnol. 2016, 32, 177. [Google Scholar] [CrossRef] [PubMed]
  44. Tang, H.; Zhao, L.; Sun, W.; Hu, Y.; Han, H. Surface characteristics and wettability enhancement of respirable sintering dust by nonionic surfactant. Colloids Surf. A Physicochem. Eng. Asp. 2016, 509, 323–333. [Google Scholar] [CrossRef]
  45. Beekman, P.; Enciso-Martinez, A.; Pujari, S.P.; Terstappen, L.; Zuilhof, H.; le Gac, S.; Otto, C. Author Correction: Organosilicon uptake by biological membranes. Commun. Biol. 2021, 4, 704, Erratum in Commun. Biol. 2021, 4, 812. [Google Scholar] [CrossRef]
  46. Yuan, M.; Nie, W.; Zhou, W.; Yan, J.; Bao, Q.; Guo, C.; Tong, P.; Zhang, H.; Guo, L. Determining the effect of the non-ionic surfactant AEO9 on lignite adsorption and wetting via molecular dynamics (MD) simulation and experiment comparisons. Fuel 2020, 278, 118–339. [Google Scholar] [CrossRef]
  47. Banat, I.M.; Franzetti, A.; Gandolfi, I.; Bestetti, G.; Martinotti, M.G.; Fracchia, L.; Smyth, T.J.; Marchant, R. Microbial biosurfactants production, applications and future potential. Appl. Microbiol. Biotechnol. 2010, 87, 427–444. [Google Scholar] [CrossRef] [PubMed]
  48. Chen, L.; Shi, H.; Wu, H.; Xiang, J. Synthesis and combined properties of novel fluorinated anionic surfactant. Colloids Surf. A Physicochem. Eng. Asp. 2011, 384, 331–336. [Google Scholar] [CrossRef]
  49. Huang, G.; Deng, Y.; Zhang, Y.; Feng, P.; Xu, C.; Fu, L.; Lin, B. Study on long-term pest control and stability of double-layer pesticide carrier in indoor and outdoor environment. Chem. Eng. J. 2021, 403, 126–342. [Google Scholar] [CrossRef]
  50. Singh, A.; Dhiman, N.; Kar, A.K.; Singh, D.; Purohit, M.P.; Ghosh, D.; Patnaik, S. Advances in controlled release pesticide formulations: Prospects to safer integrated pest management and sustainable agriculture. J. Hazard. Mater. 2020, 385, 121525. [Google Scholar] [CrossRef] [PubMed]
  51. Kashyap, P.L.; Xiang, X.; Heiden, P. Chitosan nanoparticle based delivery systems for sustainable agriculture. Int. J. Biol. Macromol. 2015, 77, 36–51. [Google Scholar] [CrossRef]
  52. Patra, J.K.; Das, G.; Fraceto, L.F.; Campos, E.V.R.; Rodriguez-Torres, M.D.P.; Acosta-Torres, L.S.; Diaz-Torres, L.A.; Grillo, R.; Swamy, M.K.; Sharma, S.; et al. Nano based drug delivery systems: Recent developments and future prospects. J. Nanobiotechnology 2018, 16, 71. [Google Scholar] [CrossRef] [Green Version]
  53. Mohammadzadeh Kakhki, R.; Karimian, A.; Saadati Rad, M. Highly efficient removal of paraquat pesticide from aqueous solutions using a novel nano Kaolin modified with sulfuric acid via host–guest interactions. J. Incl. Phenom. Macrocycl. Chem. 2020, 96, 307–313. [Google Scholar] [CrossRef]
  54. Shan, Y.; Xu, C.; Zhang, H.; Chen, H.; Bilal, M.; Niu, S.; Cao, L.; Huang, Q. Polydopamine-modified metal–organic frameworks, NH2-Fe-MIL-101, as pH-sensitive nanocarriers for controlled pesticide release. Nanomaterials 2020, 10, 2000. [Google Scholar] [CrossRef] [PubMed]
  55. Tong, Y.; Wu, Y.; Zhao, C.; Xu, Y.; Lu, J.; Xiang, S.; Zong, F.; Wu, X. Polymeric Nanoparticles as a Metolachlor Carrier: Water-Based Formulation for Hydrophobic Pesticides and Absorption by Plants. J. Agric. Food Chem. 2017, 65, 7371–7378. [Google Scholar] [CrossRef] [PubMed]
  56. Xu, C.; Qi, J.; Yang, W.; Chen, Y.; Yang, C.; He, Y.; Wang, J.; Lin, A. Immobilization of heavy metals in vegetable-growing soils using nano zero-valent iron modified attapulgite clay. Sci. Total Environ. 2019, 686, 476–483. [Google Scholar] [CrossRef] [PubMed]
  57. Xu, L.; Cao, L.D.; Li, F.M.; Wang, X.J.; Huang, Q.L. Utilization of Chitosan-Lactide Copolymer Nanoparticles as Controlled Release Pesticide Carrier for Pyraclostrobin Against Colletotrichum gossypii Southw. J. Dispers. Sci. Technol. 2014, 35, 544–550. [Google Scholar] [CrossRef]
  58. Purkait, A.; Hazra, D.K. Biodiesel as a carrier for pesticide formulations: A green chemistry approach. Int. J. Pest Manag. 2020, 66, 341–350. [Google Scholar] [CrossRef]
  59. Rota, E.; Healy, B. A taxonomic study of some swedish enchytraeidae (Oligochaeta), with descriptions of four new species and notes on the genus fridericia. J. Nat. Hist. 1999, 33, 29–64. [Google Scholar] [CrossRef]
  60. Zhang, H.; Chen, W.; Zhao, B.; Phillips, L.A.; Zhou, Y.; Lapen, D.R.; Liu, J. Sandy soils amended with bentonite induced changes in soil microbiota and fungistasis in maize fields. Appl. Soil Ecol. 2020, 146, 103–378. [Google Scholar] [CrossRef]
  61. Lei, Y.; Liu, X.; Li, S.; Jiang, L.; Zhang, C.; Li, S.; He, D.; Wang, S. High stability of palladium/kieselguhr composites during absorption/desorption cycling for hydrogen isotope separation. Fusion Eng. Des. 2016, 113, 260–264. [Google Scholar] [CrossRef]
  62. Maghsoodi, M.R.; Najafi, N.; Reyhanitabar, A.; Oustan, S. Hydroxyapatite nanorods, hydrochar, biochar, and zeolite for controlled-release urea fertilizers. Geoderma 2020, 379, 114644. [Google Scholar] [CrossRef]
  63. Dutta, J.; Devi, N. Preparation, optimization, and characterization of chitosan-sepiolite nanocomposite films for wound healing. Int. J. Biol. Macromol. 2021, 186, 244–254. [Google Scholar] [CrossRef]
  64. Xiang, Y.; Lu, X.; Yue, J.; Zhang, Y.; Sun, X.; Zhang, G.; Cai, D.; Wu, Z. Stimuli-responsive hydrogel as carrier for controlling the release and leaching behavior of hydrophilic pesticide. Sci. Total Environ. 2020, 722, 137811. [Google Scholar] [CrossRef]
  65. Heris Anita, S.; Mangunwardoyo, W.; Yopi, Y. Sugarcane Bagasse as a Carrier for the Immobilization of Saccharomyces cerevisiaein Bioethanol Production. Makara J. Technol. 2016, 20, 73. [Google Scholar] [CrossRef] [Green Version]
  66. Haider, M.; Abdin, S.M.; Kamal, L.; Orive, G. Nanostructured Lipid Carriers for Delivery of Chemotherapeutics: A Review. Pharmaceutics 2020, 12, 288. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  67. Dos Santos, C.A.M.; do Nascimento, J.; Gonçalves, K.C.; Smaniotto, G.; de Freitas Zechin, L.; da Costa Ferreira, M.; Polanczyk, R.A. Compatibility of Bt biopesticides and adjuvants for Spodoptera frugiperda control. Sci. Rep. 2021, 11, 5271. [Google Scholar] [CrossRef]
  68. Li, J.; Yao, J.; Li, Y.; Shao, Y. Controlled release and retarded leaching of pesticides by encapsulating in carboxymethyl chitosan /bentonite composite gel. J. Environ. Sci. Health - Part B Pestic. Food Contam. Agric. Wastes 2012, 47, 795–803. [Google Scholar] [CrossRef]
  69. Voinova, O.N.; Kalacheva, G.S.; Grodnitskaya, I.D.; Volova, T.G. Microbial polymers as a degradable carrier for pesticide delivery. Appl. Biochem. Microbiol. 2009, 45, 384–388. [Google Scholar] [CrossRef]
  70. Jarzębski, M.; Smułek, W.; Siejak, P.; Kobus-Cisowska, J.; Pieczyrak, D.; Baranowska, H.M.; Jakubowicz, J.; Sopata, M.; Białopiotrowicz, T.; Kaczorek, E. Aesculus hippocastanum L. extract as a potential emulsion stabilizer. Food hydrocolloids. 2019, 54, 68. [Google Scholar] [CrossRef]
  71. Jadhav, N.; Pantwalawalkar, J.; Sawant, R.; Attar, A.; Lohar, D.; Kadane, P.; Ghadage, K. Development of Progesterone Oily Suspension Using Moringa Oil and Neusilin US2. J. Pharm. Innov. 2021, 21, 79. [Google Scholar] [CrossRef]
  72. Kaur, R.; Thakur, N.S.; Chandna, S.; Bhaumik, J. Development of agri-biomass based lignin derived zinc oxide nanocomposites as promising UV protectant-cum-antimicrobial agents. J. Mater. Chem. 2020, 8, 260–269. [Google Scholar] [CrossRef] [PubMed]
  73. Sukirno, S.; Lukmawati, D.; Hanum, S.S.L.; Ameliya, V.F.; Sumarmi, S.; Purwanto, H.; Suparmin, S.; Sudaryadi, I.; Soesilohadi, R.C.H.; Aldawood, A.S. The effectiveness of Samia ricini Drury (Lepidoptera: Saturniidae) and Attacus atlas L. (Lepidoptera: Saturniidae) cocoon extracts as ultraviolet protectants of Bacillus thuringiensis for controlling Spodoptera litura Fab. (Lepidoptera: Noctuidae). Int. J. Trop. Insect Sci. 2022, 42, 255–260. [Google Scholar] [CrossRef]
  74. Pershakova, T.V.; Gorlov, S.M.; Lisovoy, V.V.; Mikhaylyuta, L.V.; Babakina, M.V.; Aleshin, V.N. Influence of electromagnetic fields and microbial pesticide Vitaplan on stability of apples during storage. IOP Conf. Ser. Earth Environ. Sci. 2021, 640, 022053. [Google Scholar] [CrossRef]
  75. Zhang, J.; Wang, W.; Pei, Z.; Wu, J.; Yu, R.; Zhang, Y.; Sun, L.; Gao, Y. Mutagenicity assessment to pesticide adjuvants of toluene, chloroform and trichloroethylene by ames test. Int. J. Environ. Res. Public Health 2021, 18, 8095. [Google Scholar] [CrossRef]
  76. Wang, G.; Chen, H.; Wang, X.; Peng, L.; Peng, Y.; Li, Y.-Q. Probing the germination kinetics of ethanol-treated Bacillus thuringiensis spores. Appl. Opt 2017, 56, 3263–3269. [Google Scholar] [CrossRef]
  77. Ruiu, L.; Satta, A.; Floris, I.; Floris, I. Administration of Brevibacillus laterosporus spores as a poultry feed additive to inhibit house fly development in feces: A new eco-sustainable concept. Poult. Sci. 2014, 93, 519–526. [Google Scholar] [CrossRef] [PubMed]
  78. Whalon, M.E.; Wingerd, B.A. Bt: Mode of action and use. Arch. Insect Biochem. Physiol. 2003, 54, 200–211. [Google Scholar] [CrossRef] [PubMed]
  79. Gómez, J.; Guevara, J.; Cuartas, P.; Espinel, C.; Villamizar, L. Microencapsulated Spodoptera frugiperda nucleopolyhedrovirus: Insecticidal activity and effect on arthropod populations in maize. Biocontrol Sci. Technol. 2013, 23, 829–846. [Google Scholar] [CrossRef]
  80. Taylor, P.; Soe, K.T.; De Costa, D.M. Development of a spore-based formulation of microbial pesticides for control of rice sheath blight. Biocontrol Sci. Technol. 2012, 22, 633–657. [Google Scholar]
  81. Pratap, A.P.; Bhowmick, D.N. Pesticides as microemulsion formulations. J. Dispers. Sci. Technol. 2008, 29, 1325–1330. [Google Scholar] [CrossRef]
  82. Liu, J.; He, Y.; Chen, S.; Xiao, Y.; Hu, M.; Zhong, G. Development of a freeze-dried fungal wettable powder preparation able to biodegrade chlorpyrifos on vegetables. PLoS ONE 2014, 9, e103558. [Google Scholar] [CrossRef] [PubMed]
  83. Cheng, H.; Li, L.; Hua, J.; Yuan, H.; Cheng, S. A preliminary preparation of endophytic bacteria CE3 wettable powder for biological control of postharvest diseases. Not. Bot. Horti Agrobot. 2015, 43, 159–164. [Google Scholar] [CrossRef] [Green Version]
  84. Leng, P.; Zhang, Z.; Pan, G.; Zhao, M. Applications and development trends in biopesticides. Afr. J. Biotechnol. 2011, 10, 19864–19873. [Google Scholar] [CrossRef]
  85. Samada, L.H.; Tambunan, U.S.F. Biopesticides as promising alternatives to chemical pesticides: A review of their current and future status. OnLine J. Biol. Sci. 2020, 20, 66–76. [Google Scholar] [CrossRef]
  86. Zulfitri, A.; Krishanti, N.P.R.A.; Lestari, A.S.; Meisyara, D.; Zulfiana, D. Efficacy of several entomopathogenic microorganism as microbial insecticide against insect pest on chili (Capsicum annum L.). IOP Conf. Ser. Earth Environ. Sci. 2020, 572, 012020. [Google Scholar] [CrossRef]
  87. Zhao, M.; Li, S.; Zhou, Q.; Zhou, D.; He, N.; Qian, Z. Safety evaluation of microbial pesticide (HaNPV) based on PCR method. Front. Chem. Sci. Eng. 2019, 13, 377–384. [Google Scholar] [CrossRef]
  88. Shao, H.; Zhang, Y. Non-target effects on soil microbial parameters of the synthetic pesticide carbendazim with the biopesticides cantharidin and norcantharidin. Sci. Rep. 2017, 7, 5521. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  89. Vehapi, M.; Özçimen, D. Antimicrobial and bacteriostatic activity of surfactants against B. subtilis for microbial cleaner formulation. Arch. Microbiol. 2021, 203, 3389–3397. [Google Scholar] [CrossRef]
  90. Oliveira-Hofman, C.; Cottrell, T.E.; Bock, C.; Mizell, R.F.; Wells, L.; Shapiro-Ilan, D.I. Impact of a biorational pesticide on the pecan aphid complex and its natural enemies. Biol. Control 2021, 161, 104–709. [Google Scholar] [CrossRef]
  91. Du, W.; Zhou, J.; Jiang, P.; Yang, T.; Bu, Y.Q.; Liu, C.H.; Dai, C.C. Effects of Beauveria bassiana and acephate on enzyme activities and microbial diversity in paddy soil. Plant Soil Environ. 2013, 59, 562–567. [Google Scholar] [CrossRef] [Green Version]
  92. Kumar, J.; Parmar, B.S. Stabilization of azadirachtin A in neem formulations: Effect of some solid carriers, neem oil, and stabilizers. J. Agric. Food Chem. 1999, 47, 1735–1739. [Google Scholar] [CrossRef]
  93. Brownbridge, M.; Buitenhuis, R. Integration of microbial biopesticides in greenhouse floriculture: The Canadian experience. J. Invertebr. Pathol. 2019, 165, 4–12. [Google Scholar] [CrossRef]
  94. Aslam, S.; Jahan, N.; Khalil-Ur-Rehman; Ali, S. Formulation, optimisation and in-vitro, in-vivo evaluation of surfactant stabilised nanosuspension of Ginkgo biloba. J. Microencapsul. 2019, 36, 576–590. [Google Scholar] [CrossRef]
  95. Hong, N.; Li, Y.; Qiu, X. A highly efficient dispersant from black liquor for carbendazim suspension concentrate: Preparation, self-assembly behavior and investigation of dispersion mechanism. J. Appl. Polym. Sci. 2016, 133, 1–9. [Google Scholar] [CrossRef]
  96. Vineela, V.; Nataraj, T.; Reddy, G.; Vimala Devi, P.S. Enhanced bioefficacy of Bacillus thuringiensis var. kurstaki against Spodoptera litura (Lepidoptera: Noctuidae) through particle size reduction and formulation as a suspension concentrate. Biocontrol Sci. Technol. 2017, 27, 58–69. [Google Scholar] [CrossRef]
  97. Feng, N.; Zhang, B.; Xin, X.; Li, H.; Zhao, Y. Role of aliphatic alcohol polyoxyethylene ether phosphate in 25 wt% tebuconazole suspension concentrate: Dispersion and wetting. Colloids Surf. A Physicochem. Eng. Asp. 2021, 628, 127350. [Google Scholar] [CrossRef]
  98. Wang, T.; Chen, L. Dynamic complexity of microbial pesticide model. Nonlinear Dyn. 2009, 58, 539–552. [Google Scholar] [CrossRef]
  99. Vimala Devi, P.S.; Duraimurugan, P.; Poorna Chandrika, K.S.V.; Vineela, V.; Hari, P.P. Novel formulations of Bacillus thuringiensis var. kurstaki: An eco-friendly approach for management of lepidopteran pests. World J. Microbiol. Biotechnol. 2020, 36, 78. [Google Scholar] [CrossRef] [PubMed]
  100. Kaczmarek, D.K.; Rzemieniecki, T.; Marcinkowska, K.; Pernak, J. Synthesis, properties and adjuvant activity of docusate-based ionic liquids in pesticide formulations. J. Ind. Eng. Chem. 2019, 78, 440–447. [Google Scholar] [CrossRef]
  101. Egamberdieva, D.; Jabbarov, Z.; Arora, N.K.; Wirth, S.; Bellingrath-Kimura, S.D. Biochar mitigates effects of pesticides on soil biological activities. Environ. Sustain. 2021, 4, 335–342. [Google Scholar] [CrossRef]
  102. Knowles, A. Adjuvants for agrochemicals. Pestic. Outlook 2001, 12, 183–184. [Google Scholar] [CrossRef]
  103. Shenoy, A.; Reddy, C.M.; Shree Padma, M.; Niranjan, V.; Rao, N.N. Evaluation of alternative bio-receptors for pesticide detection. Mater. Today Proc. 2018, 5, 20977–20980. [Google Scholar] [CrossRef]
  104. Fine, J.D.; Cox-Foster, D.L.; Mullin, C.A. An inert pesticide adjuvant synergizes viral pathogenicity and mortality in honey bee larvae. Sci. Rep. 2017, 7, 40499. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  105. Partners, C.R. Kline analyses US pesticide adjuvants market. Focus Surfactants 2018, 2018, 5–6. [Google Scholar] [CrossRef]
  106. Abbott, W.S. The Value of the Dry Substitutes for Liquid Lime. J. Econ. Entomol. 1925, 18, 265–267. [Google Scholar] [CrossRef]
  107. Ali, R.A.; Hasan, M.; Sagheer, M.; Sahi, S.T.; Rasul, A. Factors influencing the combined efficacy of microbial insecticides and inert dusts for the control of Trogoderma granarium. Int. J. Trop. Insect Sci. 2022, 42, 425–433. [Google Scholar] [CrossRef]
  108. Yanagisawa, K.; Muroi, T.; Ohtsubo, T.; Watano, S. Effect of binder composition on physicochemical properties of water dispersible granules obtained through direct granulation of agrochemical suspension using fluidized bed. J. Pestic. Sci. 2017, 42, 112–115. [Google Scholar] [CrossRef] [Green Version]
  109. Nile, A.S.; Kwon, Y.D.; Nile, S.H. Horticultural oils: Possible alternatives to chemical pesticides and insecticides. Environ. Sci. Pollut. Res. 2019, 26, 21127–21139. [Google Scholar] [CrossRef]
  110. Grillo, R.; Abhilash, P.C.; Fraceto, L.F. Nanotechnology applied to bio-encapsulation of pesticides. J. Nanosci. Nanotechnol. 2016, 16, 1231–1234. [Google Scholar] [CrossRef]
  111. Ryckaert, B.; Spanoghe, P.; Haesaert, G.; Heremans, B.; Isebaert, S.; Steurbaut, W. Quantitative determination of the influence of adjuvants on foliar fungicide residues. Crop Prot. 2007, 26, 1589–1594. [Google Scholar] [CrossRef]
  112. Mansour, R.; Biondi, A. Releasing natural enemies and applying microbial and botanical pesticides for managing Tuta absoluta in the MENA region. Phytoparasitica 2021, 49, 179–194. [Google Scholar] [CrossRef]
Figure 1. Micelle formation and surface adsorption of surfactants at different concentrations.
Figure 1. Micelle formation and surface adsorption of surfactants at different concentrations.
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Figure 2. Added protective agents in the microbial pesticides to avoid damage by UV rays.
Figure 2. Added protective agents in the microbial pesticides to avoid damage by UV rays.
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Table 1. Main formulations of microbial pesticides.
Table 1. Main formulations of microbial pesticides.
Main Formulations of Microbial PesticidesTypes of Microbial
Pesticides
Main Registered
Formulations
Bacillus thuringiensisBacteriumWP, SC, and WG
Bacillus licheniformisBacteriumSL
Bacillus cereusBacteriumWP and SC
Bacillus sphaericusBacteriumSC
Bacillus subtilisBacteriumWP and FS
Bacillus amyloliquefaciensBacteriumWP, SC, and WG
Bacillus velezensisBacteriumWG and TK
Bacillus firmusBacteriumWP
Bacillus marineBacteriumWP
Brevibacterium brevisBacteriumSC
Paenibacillus polymyxaBacteriumWP and SC
Pseudomonas fluorescensBacteriumWP and WG
Beauveria bassianaFungusWP
Locust MicrosporidiaFungusSC
Metarhizium anisopliaeFungusWP
Paecilomyces lilacinusFungusDP and GR
TrichodermaFungusWP and GR
Verticillium pachysporaFungusWP
Autographa californica nuclear polyhedrosis virusVirusSE
Ectropis obliqua nuclear polyhedrosis virusVirusTK
Helicoverpa armigera
nuclear polyhedrosis virus
VirusWP and SC
Mamestra brassicae
nuclear polyhedrosis virus
VirusWP, SC, GR, and TK
Plutella xylostella granulosa virusVirusWP
Pierisrapae granulosisVirusTK
Spodoptera exigua nuclear polyhedrosis virusVirusSC, WG, and TK
Spodoptera litura nuclear polyhedrosis virusVirusWP, SC, and WG
Wettable powder(WP), suspension concentration(SC), dispersible granules(WG), soluble liquid(SL), seed treatment(FS), granules(GR), powder(DP), technical concentration(TK).
Table 3. Carriers commonly used for the production of microbial pesticides.
Table 3. Carriers commonly used for the production of microbial pesticides.
Types of CarriersFeaturesReferences
BentoniteIts main component is montmorillonite, which has strong adsorption and large specific surface area. After absorbing a large number of water molecules, it expands and splits into extremely fine particles.[60]
DiatomiteIts main component is SiO2, which harbors many micropores and has a capacity of low relative density, high porosity, and strong adsorption. It is widely used in the manufacture of high-concentration powder carriers.[61]
Attapulgite clayIts main component is attapulgite, which has a capacity of strong adsorption and a property of large specific surface area and unique thickening. It is widely used in the manufacture of high-concentration powder carriers and granule substrates, as well as thickeners for suspensions.[57]
KaolinIts main component is kaolinite, which has a relatively compact structure, a small specific surface area, and an adsorption capacity. It is often used as a carrier for low-concentration powders, and the price is relatively cheap.[57]
ZeoliteActive ingredients in forms of porous hydrous aluminosilicate crystals are highly adsorbable to certain polar molecules such as zeolite and then slowly released. It is often used as a carrier for sustained-release granules.[62]
SepioliteIts main component is magnesium-rich fibrous clay minerals with large porosity and specific surface area. It can absorb liquid and low-melting pesticides. Because of its light weight, it can float on the water surface.[63]
Synthetic vectorsMost of them are made with light calcium carbonate and white carbon black, which have strong specific surface area and adsorption capacity, and can be used as a carrier for high concentration powders.[64]
Plant vectorsMost of them are made with bagasse, corn bagasse, chaff powder, tobacco powder, and walnut shell powder. Plant-based carriers are rarely used at present. Some of them have special properties such as absorbing ultraviolet (UV) rays.[65]
Nanostructured Lipid CarriersThey have excellent permeability, retention, targeting, stability, and can reduce or eliminate the side effects of active ingredients, with good slow release and controlled release properties.[66]
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Lin, F.; Mao, Y.; Zhao, F.; Idris, A.L.; Liu, Q.; Zou, S.; Guan, X.; Huang, T. Towards Sustainable Green Adjuvants for Microbial Pesticides: Recent Progress, Upcoming Challenges, and Future Perspectives. Microorganisms 2023, 11, 364. https://doi.org/10.3390/microorganisms11020364

AMA Style

Lin F, Mao Y, Zhao F, Idris AL, Liu Q, Zou S, Guan X, Huang T. Towards Sustainable Green Adjuvants for Microbial Pesticides: Recent Progress, Upcoming Challenges, and Future Perspectives. Microorganisms. 2023; 11(2):364. https://doi.org/10.3390/microorganisms11020364

Chicago/Turabian Style

Lin, Fuyong, Yufei Mao, Fan Zhao, Aisha Lawan Idris, Qingqing Liu, Shuangli Zou, Xiong Guan, and Tianpei Huang. 2023. "Towards Sustainable Green Adjuvants for Microbial Pesticides: Recent Progress, Upcoming Challenges, and Future Perspectives" Microorganisms 11, no. 2: 364. https://doi.org/10.3390/microorganisms11020364

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