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Review

The Potential of Adjuvants Used with Microbiological Control of Insect Pests with Emphasis on Organic Farming

by
Małgorzata Holka
and
Jolanta Kowalska
*
Department of Organic Agriculture and Environmental Protection, Institute of Plant Protection—National Research Institute, Władysława Węgorka 20, 60-318 Poznań, Poland
*
Author to whom correspondence should be addressed.
Agriculture 2023, 13(9), 1659; https://doi.org/10.3390/agriculture13091659
Submission received: 31 July 2023 / Revised: 18 August 2023 / Accepted: 21 August 2023 / Published: 23 August 2023
(This article belongs to the Special Issue Integrated Management of Crop Diseases and Pests)
Review Reports Versions Notes

Abstract

:
Biological plant protection is a crucial component of integrated pest management strategies. It is considered a safer alternative to chemical plant protection, with reduced risks to human health and the environment. The significance of biological plant protection has been on the rise, driven by the European Union’s mandate to decrease the reliance on chemical pesticides, the discontinuation of certain chemical active substances, and their limited availability. Microbiological plant protection products find application in organic farming systems. Among these, mycoinsecticides are prominent examples, utilizing insecticidal fungi such as Beauveria bassiana, Cordyceps fumosoroseus, C. farinosa, and Metarhizium anisopliae complex. Due to the high sensitivity of these organisms to unfavorable weather and environmental conditions, their use in the protection of field crops may not bring the desired effect. The enhancement of their efficacy may be accomplished through the use of adjuvants. Adjuvants are substances incorporated into plant protection products, including microbial insecticides, or used alone to enhance their effectiveness. They can play a pivotal role in improving the performance of mycoinsecticides by ensuring better coverage on plant surfaces and increasing the likelihood of successful pest control, thereby contributing to the overall success of biological methods of pest control. Consequently, it becomes imperative to investigate the impact of various adjuvants on the survival and effectiveness of microorganisms. Furthermore, there is no officially approved list of adjuvants for use in organic farming, the use of inadequate adjuvant may result in failure to obtain an organic certificate. The origin of adjuvants determines their classification, which significantly impacts for employment in organic farming practices. Included tables provide a list of adjuvants and additives known to enhance the efficacy of pest and disease control.

1. Introduction

Crop pests are common in plant crops and can inflict significant damage. Global crop production is estimated to suffer losses of up to 40 percent each year due to their activities [1,2,3]. Ensuring adequate protection of crops is essential for maintaining food security and the profitability of crop production [4]. Various methods are used to protect plants, including chemical, agrotechnical, mechanical, physical, biological, breeding, integrated and quarantine methods. Among them, the most commonly used method is chemical plant protection [5]. Its popularity stems from its high efficiency and cost-effectiveness [6]. The utilization of chemical plant protection products facilitates the attainment of optimal plant yields and high-quality produce. However, it is important to acknowledge that their use is accompanied by adverse environmental consequences [7,8,9]. Over 90% of the applied agents in chemical treatments disperse into the environment [10]. Reducing the reliance on chemical plant protection products is crucial to mitigate the risks of environmental pollution, biodiversity depletion, and the development of pest resistance to chemical substances [11].
Since 2014, the European Union (EU) has enforced a legal obligation to adhere to the principles of Integrated Pest Management (IPM), as outlined in Directive 2009/128/EC [6,12]. In accordance with IPM guidelines, the utilization of chemical plant protection products should be restricted to the bare minimum, while prioritizing the extensive implementation of non-chemical alternatives [13]. Biological plant protection emerges as one such approach covering control, prevention, and eradication of plant pests through the utilization of biological agents. These agents include compounds derived from plants and animals, viruses, bacteria, protozoa, fungi, mites, and insects, which serve as the active substances in biological plant protection products [14,15]. The use of preparations of natural origin or containing living organisms with antagonistic properties against pests not only minimizes the negative impact of plant production on the environment, but also ensures food production without residues of chemical plant protection products [16,17,18].
Furthermore, the challenges in plant protection are compounded by the diminishing availability of active substances authorized for marketing and use in the EU [19]. A significant hurdle in plant production and protection arises from the mandatory reduction in chemical plant protection product usage by 50 percent by 2030 in the EU, as outlined in the Farm to Fork strategy introduced by the European Commission in 2020 within the framework of the European Green Deal [20,21]. In light of these circumstances, biological plant protection products are being identified as alternative solutions to chemical counterparts [22,23,24].
Biological plant protection products find primary application in organic farming (OF) systems, where the use of chemical active substances is prohibited. In conventional production systems, their reduced adoption is primarily attributed to higher costs and slower efficacy compared to chemical plant protection products [14]. Furthermore, the application of biological plant protection products, particularly microbiological preparations, is challenging due to the vulnerability of contained microorganisms to environmental factors such as sunlight, temperature, and humidity [25,26]. Satisfactory outcomes from microbiological preparations are often observed in crops cultivated under controlled conditions, such as those grown in covered environments [27]. In Poland, there is a potential increase in interest regarding the utilization of microbiological preparations in agriculture, as agricultural producers now have the opportunity to receive subsidies for direct payments by voluntarily committing to implementing biological crop protection practices on their farms, under the “Biological pest control” eco-scheme introduced from 2023 [28].
The advancement of sustainable plant production technologies necessitates the development of novel plant protection products characterized by low toxicity to non-target organisms and high biodegradability [29,30,31]. Biopreparations fulfill these criteria, exemplified by mycoinsecticides that utilize entomopathogenic fungi such as Beauveria bassiana, Cordyceps fumosorosea (formerly Isaria fumosorosea or Paecilomyces fumosoroseus)), Cordyceps farinosa (formerly Isaria farinosa and Paecilomyces farinosus), and Metarhizium anisopliae complex as their active ingredients [32]. The utilization of biological insecticides, along with the incorporation of appropriate auxiliary substances, enhances their efficacy, thereby fostering increased interest in their application within plant protection practices [33]. Adjuvants added to the tank with working fluid as a separate product can also fulfill the task as auxiliary.
The efficacy of plant protection measures is influenced by numerous factors, encompassing biological aspects (such as pest species, biotype, and developmental stage), environmental conditions (including air temperature, relative humidity, soil moisture, insolation, precipitation, and wind), and application-related variables (such as agent composition, formulation, dosage, water quantity and quality, physicochemical properties of the spray solution, and treatment timing and technique) [34]. Even a single unfavorable factor can significantly diminish the effectiveness of plant protection treatments and potentially induce phytotoxicity in crops. To counteract the negative impact of these diverse factors on the efficacy of plant protection products, their use in conjunction with adjuvants and auxiliary substances is recommended [35]. In the context of chemical plant protection treatments, the incorporation of adjuvants, by influencing the physicochemical properties of the spray solution, enhances efficiency, reduces plant protection costs, and diminishes the emission of harmful active substances into the environment [36]. Adjuvants also play a crucial role in the production and application of biological plant protection products, augmenting their durability and effectiveness [26].
The market for adjuvants is experiencing dynamic growth. Currently, approximately 150 adjuvant products are available in Poland, as reported in [37]. However, due to the lack of adjuvant registration in Poland, precise categorization of these products remains challenging. Consequently, access to reliable information regarding the available range of adjuvants, their compositions, and appropriate selection criteria is limited. Unlike plant protection products, which have a dedicated database containing comprehensive information and labels, Poland does not possess a similar database for adjuvants. Furthermore, there is no officially approved list of adjuvants for use in organic farming. According to Article 9(3) of Regulation (EU) 2018/848, safeners, synergists, co-formulants as components of plant protection products, and adjuvants intended for mixture with plant protection products may be permitted for use in organic production, provided they are authorized in accordance with Regulation (EC) No 1107/2009 [38,39]. The substances listed in this Annex may only be utilized for the control of pests as defined in Article 3(24) of Regulation (EU) 2018/848. The registration of adjuvants based on reliable research pertaining to their effectiveness in plant protection treatments and their safety for the environment and humans would greatly contribute to the systematic classification of these products. Furthermore, it would provide invaluable and trustworthy information for both conventional and especially organic producers.
This study presents a comprehensive review of the potential for synergistic of employing adjuvants with biological plant protection products, with a specific focus on those containing entomopathogenic fungi.

2. Biopreparations in Plant Protection

Biological protection products, along with biofertilizers and biostimulators, constitute a category of bioproducts specifically intended for application in plant production [40]. They include (1) biopesticides containing (i) biochemicals such as extracts, active molecules of plant origin (e.g., azadirachtin, plant oils, pyrethrins) and compounds of animal origin, i.e., semi-compounds such as pheromones, allomonos, kairomones, and (ii) microorganisms including bacteria, fungi, viruses, and protozoa, and (2) macroorganisms such as parasitic mites, hyperparasitic and predator insects, and entomopathogenic nematodes [41].
These biological agents are utilized for the suppression and regulation of diverse pest groups, specifically targeting insects (bioinsecticides), mites (bioacaricides), nematodes (bionematocides), fungi (biofungicides), weeds (bioherbicides), and bacteria (biobactericides).
Microbiological preparations constitute a significant category of biological plant protection products. These preparations contain microorganisms as active ingredients, which must undergo approval for usage in plant protection products and be included in the Union list of active substances. Presently, the European Union (EU) has approved 75 microorganism-based active substances for plant protection products (as of 27 May 2023) [42]. The majority of microbiological preparations are designed for combating insect pests and pathogenic fungi, with fungi and bacteria being the dominant constituents. The list of active substances approved in the EU includes 12 strains of insecticidal fungi (Table 1). In Poland, the register of plant protection products encompasses 8 mycoinsecticides (Table 2). Despite their significance, microbiological preparations currently account for a mere 2% of the total plant protection product market in Poland [43]. However, it is anticipated that their assortment will expand due to the regulatory measures introduced by the EU in 2022 concerning the registration procedures for plant protection products containing microorganisms [31,44].

3. Adjuvants for Biopesticides

An adjuvant is a substance, or a mixture of substances of natural or synthetic origin incorporated into a plant protection product’s (PPPs) formulation or used together with PPPs if they are not part of the composition. with the purpose of enhancing the efficacy of the plant protection treatment through modification of the active substance’s biological properties or the physicochemical characteristics of the working solution [35].
The utilization of auxiliary substances in plant protection can be traced back to the 18th century when various additives such as resin, tar, flour, molasses, and sugar were employed alongside lime, sulfur, copper, and arsenic to enhance adhesion and efficacy [45,46]. Notably, in 1877, a mixture of mineral oil and soap was employed in the United States to eliminate aphid eggs, while soaps derived from fish and whale fat were incorporated into pesticides towards the end of the 19th century. During the early 20th century, the most commonly utilized additives in plant protection treatments encompassed soaps, oils, glucose, casein, and molasses [47]. Presently, adjuvants find widespread application in agriculture for plant protection and foliar fertilization purposes [46,48].
Adjuvants can be categorized based on diverse criteria, such as their origin, chemical structure of particles, or mechanism of action. In relation to their roles in plant protection treatments, distinct classifications have been established for activating, modifying, and multifunctional adjuvants [34,37,49,50].
In the production of microbiological preparations, four distinct types of auxiliary substances have been utilized: (1) surfactants are employed to diminish the surface tension of the liquid, thereby enhancing the wetting ability of the treated surface, (2) carriers play a pivotal role in the controlled release of active ingredients in a timely manner, (3) protective agents safeguard microorganisms contained in biopreparations against unfavorable environmental conditions, and (4) nutrients are employed to provide essential nourishment to microorganisms present in biopreparations [26].
Certain adjuvants can be derived from renewable raw materials, further emphasizing their environmental compatibility. When produced through environmentally friendly processes, they are commonly referred to as “green”. According to [51], “green adjuvants” are compounds that exhibit minimal impact on both human health and the environment. They do not contribute to increased mobility of active substances in the environment and do not escalate the toxicity of active substances towards humans, inert organisms, or beneficial organisms. Furthermore, they enhance the efficacy of active substances, enabling a reduction in the required dose of plant protection products. The origin of auxiliary substances determines their classification into either natural or synthetic variants. This classification significantly impacts their suitability for employment in organic farming practices. Table 3 provides a list of adjuvants and additives known to enhance the efficacy of pest and disease control. These substances hold potential for utilization in organic farming, on the condition that they originate from natural sources.

3.1. Surfactants for Biocontrol Agents

Surface active agents, also known as surfactants, belong to a group of surface active compounds characterized by their amphiphilic nature. These molecules consist of two distinct parts: a hydrophilic and lipophobic “head” region, and a hydrophobic and lipophilic “tail” region. The hydrophilic portion exhibits a strong affinity towards polar liquids, such as water and hydrophilic water-soluble substances. Conversely, the hydrophobic segment demonstrates an affinity for non-polar liquids, including fats, waxes, and lipophilic fat-soluble substances [62].
The hydrophilic–lipophobic properties of surfactants facilitate the transfer of substances from the aqueous spray liquid (water environment) to the waxy protective layer (fat environment) that covers the bodies of insects and the surfaces of above-ground plant parts. Notably, surfactants possess a remarkable ability to reduce the surface tension of the solution in which they are present. As the concentration of surfactants increases, the surface tension of the solution decreases until it reaches the Critical Micelle Concentration (CMC). Beyond the CMC, surfactant molecules aggregate and form micelles [54,62]. Another parameter that characterizes the properties of surfactants is their degree of polarity, which is expressed by the hydrophilic–lipophilic balance (HLB) indicator. The HLB of a specific surfactant is determined by the size and strength of its hydrophilic and lipophilic groups. Lower HLB values indicate greater solubility in oil (non-polar), whereas higher HLB values indicate greater solubility in water (polar). Based on the HLB indicator, surfactants are classified into different categories: water/oil emulsifiers (HLB value ranging from 4 to 6), wetting agents (HLB value ranging from 7 to 9), oil/water emulsifiers (HLB value ranging from 8 to 18), detergents (HLB value ranging from 13 to 15), and solubilizers (HLB value ranging from 15 to 18) [63].
Elevated surface tension of a liquid results in a more spherical shape of droplets, which is deemed unfavorable. Such droplet shape restricts direct contact with the surface, leading to easy runoff. However, the solubility of surfactant molecules in both water and fat allows them to float to the surface and break the hydrogen bonds between water molecules. This process leads to a reduction in the water droplet’s surface tension and its flattening. Consequently, the spray liquid acquires enhanced coverage over a broader area of plant or pest surfaces, facilitating easier penetration [34].
The classification of surfactants into ionic and non-ionic compounds is contingent upon the molecular structure and the hydrophilic portion’s potential for electrolytic dissociation in an aqueous solution. Ionic surfactants encompass anionic, cationic, and amphoteric compounds [64].
Anionic surfactants are compounds whose hydrophilic group is a carrier of a negative charge. The polar part of their molecules are usually carboxylate, sulfate, sulfonate and phosphate groups. Anionic surfactants are characterized by biodegradability and low phytotoxicity. They are often combined with chemical plant protection products with contact action. Their production is relatively easy and low-cost [65].
Cationic surfactants possess a hydrophilic group characterized by a positive charge. This category encompasses amine salts, ammonium base salts, nitrogen base salts, as well as base salts lacking a nitrogen molecule within their structure. Owing to their pronounced phytotoxicity, the utilization of cationic surfactants in plant protection applications is not recommended. Instead, they find widespread usage in the formulation of detergents and cosmetics. The production processes associated with cationic surfactants are notably intricate and costly [64].
Amphoteric surfactants incorporate hydrophilic groups that carry both positive and negative charges within their molecular structure. This unique attribute allows them to interact with a diverse range of substances. However, the application of amphoteric surfactants is limited primarily due to their high production costs [64].
Non-ionic surfactants lack the ability to undergo electrolytic dissociation in aqueous solutions. Their molecular structure comprises hydrophilic groups with a neutral charge that are connected to hydrocarbon chains (hydrophobic groups). Within this group, compounds exhibit variations in chain length and the presence of double bonds. Depending on their specific chemical structure, non-ionic surfactants perform diverse functions as adjuvants. They can originate from natural sources or be synthetically produced. Among the commonly employed non-ionic surfactants are sorbitan esters and their ethoxylated derivatives, which are commercially available in the form of Tween 80. Non-ionic surfactants demonstrate compatibility with plant protection products exhibiting different mechanisms of action. They facilitate enhanced penetration of plant protection products without inducing damage to crop tissues. Furthermore, they can be utilized across a wide range of environmental conditions. Within the realm of agriculture, non-ionic surfactants represent the most extensively employed surfactant group. This group encompasses various surfactants, such as organosilicon and silicone surfactants, as well as select biosurfactants such as saponins [46,52].

3.2. Oil Adjuvants

Oil adjuvants, encompass a range of vegetable oils (e.g., rapeseed, sunflower, soybean) and their derivatives (e.g., free fatty acids extracted from vegetable oils, methyl or ethyl esters of free fatty acids derived from vegetable oils), as well as mineral oils, predominantly paraffin, obtained during the oil refining process. These adjuvants contribute to enhanced solubility of active substances, increased solubility of the plant and pest wax layer, and improved adhesion of plant protection products. Moreover, oil adjuvants effectively delay the drying process of the applied agents on the treated surface, facilitating deeper penetration of active substances into pest cells. Oil-based adjuvants incorporate surfactants that effectively reduce surface tension. A well-selected surfactant functions as an emulsifier, enabling the homogeneous dispersion of oil in water; however, all are not appropriate for organic farming. There are two types of emulsifiable oil adjuvants, namely crop oils and crop oil concentrates (COC). Crop oils contain up to 5 percent surfactant, while COCs may contain up to 20 percent surfactant and are used primarily with herbicides that target grasses [49]. It is advised to avoid using plant oil adjuvants under conditions of high ambient temperatures to mitigate the risk of phytotoxicity [37]. It is important to note that the efficacy of vegetable oil-based adjuvants is diminished by solar radiation. Nevertheless, it is essential to recognize that oils assume a pivotal role in plant protection strategies. Notably, oils serve as insecticides, effectively targeting a range of soft-bodied insect pests, such as mites, aphids, whiteflies, thrips, mealybugs, and scale insects. They can effectively target the egg stage of insects by either disrupting the normal exchange of gases through the egg surface or interfering with the egg’s structural integrity. When used against other stages of insects, oils have the capacity to obstruct the respiratory system, leading to suffocation or breakdown of the insect’s cuticle [29].

3.3. Biopolymers

Polymers represent another group of compounds utilized to enhance the effectiveness of biological plant protection products. In organic farming, only natural polymers (biopolymers) derived from plant and animal sources are permissible. These compounds encompass polysaccharides, polypeptides, and proteins. Various polysaccharides such as chitin, chitosan, alginates, gellan gum, cellulose derivatives, galactoglucomannans, and lignins are employed in treatments aimed at improving sowing materials in organic farming [66,67]. Biopolymers can also serve as carriers of active substances or microorganisms in biological plant protection [68,69]. These compounds can coalesce and form a protective film to prevent spray droplets from evaporating or being washed away by rain, as well as increase the viscosity of the working solution [59,70,71].

3.4. Humus Substances

Humus substances are natural organic compounds formed through the decomposition of organic matter and the synthesis activity of microorganisms. They can be classified into two main groups: humic acids and fulvic acids. These substances have a positive impact on soil quality and plant health. Humus substances stimulate the release of organic acids from plant roots, which serve as nutrients for beneficial microorganisms. This, in turn, enhances plant root growth and colonization by microorganisms, providing benefits for both plant and soil health and are desirable to use in OF [72]. Both humic acid and fulvic acid are known for their chelating effect, which allows them to encapsulate micronutrients, as well as their ability to retain moisture due to their hygroscopic and humectant properties [70]. They can also serve as carriers for microorganisms [73]. Humic acid is recognized as a biocompatible, environmentally friendly, and cost-effective biosurfactant [74]. Additionally, it is known to provide protection against ultraviolet (UV) radiation [60]. As for fulvic acids, their synergistic effect with beneficial microorganisms in reducing fungal diseases in plants has been demonstrated [75].

4. The Influence of Various Adjuvants and Additives on the Effectiveness of Mycoinsecticides

Literature research confirms the impact of combining some additives and mycoinsecticides on increased efficiency plant protection treatments. Table 4 presents examples of the beneficial effects of various additives on the activity of entomopathogenic fungi, such as B. bassiana, C. fumosoroseus, and M. anisopliae complex, in plant protection.
Preparations encompassing entomopathogenic fungi necessitate the inclusion of surfactants to enhance their wettability and mitigate particle aggregation when deployed in aquatic environments. The selection of surfactants is of utmost importance to ensure the preservation of fungal viability. Gatarayiha et al. [76] conducted a comprehensive investigation into the compatibility of a silicone surfactant, namely Break-Thru, and a mineral oil-based adjuvant comprising paraffin oil with an emulsifier, with the entomopathogenic fungus B. bassiana. Furthermore, the efficacy of the combination of each of these adjuvants with the fungus in managing the spider mite Tetranychus urticae in greenhouse vegetable crops (e.g., cucumber, tomato, eggplant, and green bean) was evaluated. The research findings revealed that employment of a silicone surfactant led to a greater survival rate of B. bassiana conidia compared to the use of an oil adjuvant. Additionally, the utilization of a silicone surfactant enhanced the effectiveness of the biopreparation containing B. bassiana, resulting in a higher spider mite mortality when compared to treatment with a mineral oil-based adjuvant.
Loeblein et al. [77] assessed the efficacy of controlling Gyropsylla spegazziniana in yerba mate (Ilex paraguariensis St.-Hil.) cultivation using a biopreparation comprising B. bassiana, in combination with an adjuvant based on soybean oil and an adjuvant based on mineral oil. The application of the biopreparation with both adjuvants resulted in elevated mortality rates of G. spegazziniana, reaching approximately 65% and 75%, respectively, in contrast to a 47% mortality rate observed when using the biopreparation without an adjuvant. Both adjuvants demonstrated compatibility with B. bassiana and did not induce any phytotoxic effects in the crop cultivation process.
The compatibility of rapeseed oil with the entomopathogenic fungus B. bassiana was investigated in [78], yielding significant research findings. The concurrent application of the fungus with rapeseed oil exhibited a synergistic effect, resulting in an augmented mortality rate of beetles compared to the use of individual substances. Conversely, the combination of B. bassiana treatment with stone dust displayed a reduced efficacy in pest mortality when compared to the effect of using the substances individually. Therefore, special attention should be paid to the fact that the use of the wrong adjuvant or in the spray liquid mixture or the addition of the wrong co-formulant to the composition of the bio-product may contribute to a reduction in the viability or effectiveness of the beneficial organism.
Swathi et al. [79] conducted a comprehensive study examining the impact of various adjuvants (Tween 20, Tween 40, Tween 60, Tween 80, Triton-X, glycerol, kaolite, silica gel, sunflower oil, neem oil, pongamia oil) on B.bassiana. Among the tested adjuvants, carboxymethyl cellulose exhibited the least inhibition of fungal growth, followed by kaolite and silica gel. The authors highlighted the beneficial effects of incorporating carboxymethyl cellulose into the formulation of B. bassiana.
In a study in [80], the compatibility of eight adjuvants (Tween 80, glycerol, neem oil, neem soap, carboxymethyl cellulose, silica gel, sunflower oil, and peanut oil) with the entomopathogenic fungus M. anisopliae complex was assessed. The application of each adjuvant inhibited the growth of M. anisopliae complex mycelium. Notably, carboxymethyl cellulose resulted in the highest mycelium growth, followed by silica gel and Neem soap. The authors emphasized that these adjuvants, particularly carboxymethyl cellulose, could enhance the stability of preparations containing M. anisopliae complex.
The impact of various vegetable oils (coconut oil, peanut oil, sesame oil, sunflower oil, neem oil, pongamia oil, and castor oil) along with two adjuvants (Laboline and Triton X 100) on the growth of the fungus C. farinosa (formerly Paecilomyces farinosus) was investigated in [81]. The study findings revealed that peanut oil, pongamia oil, sesame oil, castor oil, and Triton X 100 exerted a detrimental effect on both mycelium growth and conidia of the fungus. Conversely, sunflower oil, coconut oil, neem oil, and Laboline exhibited a positive influence on fungal development. The authors suggested that incorporating these three oils and the adjuvant could enhance the efficacy of C. farinosa in pest management. The inclusion of oils amplified the pathogenicity of the fungus by promoting conidia adhesion, augmenting durability, and enhancing infectivity against targeted pests.
One of the primary factors impeding the longevity and efficacy of B. bassiana as a biocontrol agent against insect pests is its susceptibility to solar radiation, particularly UV-A and UV-B radiation. The exposure to UV-B radiation has been observed to significantly diminish the survival rate of B. bassiana conidia [82]. In light of this, research conducted in [83] has demonstrated the potential to enhance the spore durability of B. bassiana against UV radiation by incorporating natural substances known for their UV-protective properties, namely humic acid, sesame oil, and rapeseed oil. Laboratory experiments revealed that humic acid provided more than 90% protection for B. bassiana conidia against UV-B radiation. Furthermore, field applications incorporating humic acid exhibited a persistence rate of spores at 87% after 7 days. Similarly, sesame oil and rapeseed oil exhibited high levels of UV radiation protection, surpassing 73% and 70%, respectively, in both laboratory and field settings.
The study conducted in [84] revealed a synergistic effect between kaolin and the entomopathogenic fungus B. bassiana, leading to enhanced effectiveness of the biopreparation against the Oryzaephilus surinamensis beetle.
Jackson et al. [85] investigated the impact of sucrose, zein protein, and whole milk on the stability and desiccation tolerance of stored blastospores of the insecticidal fungus Cordyceps fumosorosea. In the context of wet storage at −20 °C, the addition of whole milk to starch-oil preparations resulted in the highest survival rate of blastospores. Conversely, in the case of lyophilized starch-oil preparations, sucrose demonstrated the greatest ability to maintain blastospore viability. The inclusion of zein protein did not significantly affect the stability of C. fumosorosea.
Oliveira et al. [86] found that emulsifiable oil-based formulations can protect the conidia of B. bassiana and M. anisopliae complex from the adverse effects of high water temperatures before spraying in the field.
Luz and Batagin [87] studied the development of B. bassiana conidia when immersed in six concentrations of seven non-ionic (MP 6400, MP 600, Renex 60, Renex 95, Span 80, Tween 20 and Tween 80) and three anionic (DOS 75, Hostapaval BVQ 9 and Surfax 220) surfactants and 11 vegetable oils (linseed, soybean, groundnut, rapeseed, thistle, sunflower, olive, sesame, corn, castor, and babassu). With exception of two anionic surfactants, namely DOS 75 and Surfax 220, germination of B. bassiana conidia on complete medium was >98% at 24 h after exposure to surfactants up to 10%. Increased germination rate (>25%) was observed in 10% corn oil, milk thistle and linseed oil 8 days after incubation. The results showed that pure oils had a significant repellent effect on Triatoma infestans. The nymphs of this pest were highly susceptible to B. bassiana conidia formulated with oil and water. Adding oil to the formulation resulted in more insects succumbed to the infection than when exposed to water-formulated conidia, even at unfavorable humidity conditions for fungus growth.
Lei et al. [88] examined the effect of vegetable oils, non-ionic surfactants, and other inert ingredients (water and glycerol) on storage stability and thermal tolerance of the fungus M. anisopliae complex. They found that the oil-in-glycerol formulation was stable and able to prolong conidial shelf life.
Table 4. Examples of beneficial effect of various additives on activity of entomopathogenic fungi in plant protection.
Table 4. Examples of beneficial effect of various additives on activity of entomopathogenic fungi in plant protection.
MicroorganismsAdditivesEffectsReferences
Beauveria bassianaSilicone surfactantGreater survival rate; higher biocontrol activity[76]
Beauveria bassianaAdjuvant based on soybean oil or mineral oilHigher biocontrol activity[77]
Beauveria bassianaCarboxymethyl celluloseHigher radial growth and spore load[79]
Metarhizium anisopliae complexCarboxymethyl celluloseEnhanced stability of preparations[80]
Beauveria bassianaHumic acid, sesame oil, and rapeseed oilGreater persistence of spores[83]
Beauveria bassianaRapeseed oilHigher biocontrol activity[78]
Beauveria bassianaKaolinHigher biocontrol activity[84]
Cordyceps farinosaSunflower oil, coconut oil or neem oilHigher biocontrol activity[81]
Cordyceps fumosoroseaWhole milk or sucroseHigher survival rate[85]
Beauveria bassiana and Metarhizium anisopliae complexAdjuvant based on soybean oilIncreased tolerance of conidia to high temperature[86]
Beauveria bassianaNon-ionic and anionic surfactants, and vegetable oilsIncreased germination rate; higher biocontrol activity[87]
Metarhizium anisopliae complexVegetable oils, non-ionic surfactants, water, and glycerolEnhanced stability of prepa-rations[88]

5. Conclusions

In order to safeguard the environment and living organisms, prioritizing non-chemical methods for plant protection is imperative. Among these methods, biological plant protection holds significant importance, forming an integral part of integrated pest management and aligning with the strategies outlined in the European Green Deal. Unlike chemical plant protection products, biological plant protection products do not aim to eradicate harmful organism populations completely. Instead, they regulate these populations over an extended period due to their slower action. Consequently, complete substitution of chemical plant protection products with biopreparations is challenging. However, incorporating biopreparations into plant protection programs alongside chemical methods can mitigate losses caused by pests while reducing the reliance on chemical active substances.
The successful implementation of biological plant protection necessitates comprehensive knowledge and precise application of biopreparations. Environmental conditions pose a challenge in this regard, especially for biopreparations containing microorganisms such as entomopathogenic fungi, e.g., B. bassiana, C. fumosorosea, C. farinosa, and M. anisopliae complex that are highly sensitive to environmental factors. To overcome these challenges, adjuvants and additives can be employed to mitigate unfavorable factors in biological plant protection. Appropriately selected auxiliary substances have the potential to enhance the effectiveness of mycoinsecticides and provide a higher level of plant protection. The impact of a specific adjuvant or additive should be demonstrated through suitable tests to determine its compatibility with a particular microorganism approved for use in plant protection. There is therefore an urgent need to study the compatibility and effectiveness of various adjuvants and additives in combination with fungi used in the biological control of insect pests, as well as to assess their compatibility with the principles of organic farming. A separate issue is the distinction between commercial bioproducts intended for crop protection that contain an adjuvant in their composition, and a separate issue is the independent preparation of mixtures of mycoinsecticides with adjuvants by farmers. Often adding the wrong adjuvant can cause problems with unauthorized residues in the product and contribute to crop certification issues.
In addition to assessing the effectiveness of adjuvants and additives, data from environmental and toxicological studies are also required. To enable the use of adjuvants available on the market in organic farming, it is necessary to thoroughly evaluate their composition and ensure their registration based on regulations.

Author Contributions

Conceptualization, J.K.; investigation, M.H. and J.K.; writing—original draft preparation and editing, M.H. and J.K.; supervision, J.K. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

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Table 1. Fungal microorganisms authorized as active substances of insecticides in the European Union.
Table 1. Fungal microorganisms authorized as active substances of insecticides in the European Union.
Fungus
Akanthomyces muscarius (formerly Lecanicillium muscarium) strain Ve6
Beauveria bassiana strain PPRI 5339
Beauveria bassiana strain 147
Beauveria bassiana strain ATCC 74040
Beauveria bassiana strain GHA
Beauveria bassiana strain NPP111B005
Beauveria bassiana strains ATCC 74040 and GHA
Clonostachys rosea (also known as Gliocladium catenulatum) strain J1446
Cordyceps fumosorosea (formerly Isaria fumosorosea or Paecilomyces fumosoroseus) Apopka strain 97
Metarhizium brunneum strain Ma 43 (formerly Metarhizium anisopliae var. anisopliae)
Cordyceps fumosorosea (formerly Isaria fumosorosea or Paecilomyces fumosoroseus) strain FE 9901
Purpureocillium lilacinum (formerly Paecilomyces lilacinus) strain 251
Source: own elaboration based on data from [42].
Table 2. Currently registered plant protection products based on entomopathogenic fungi in Poland.
Table 2. Currently registered plant protection products based on entomopathogenic fungi in Poland.
ProductFungus
Futureco NoFly WPCordyceps fumosorosea (formerly Isaria fumosorosea or Paecilomyces fumosoroseus) strain Fe9901
Lalguard M52 GR NON-PROMetarhizium anisopliae var. anisopliae strain BIPESCO 5/F52
Lalguard M52 GR PROFMetarhizium anisopliae var. anisopliae strain BIPESCO 5/F52
Mycotrol 22 WPBeauveria bassiana strain GHA
Mycotrol ODBeauveria bassiana strain GHA
NaturalisBeauveria bassiana strain ATCC 74040
PreFeRalCordyceps fumosorosea (formerly Isaria fumosorosea or Paecilomyces fumosoroseus) strain Apopka 97
VeliferBeauveria bassiana strain PPRI 5339
Source: own elaboration based on data from [43].
Table 3. Selected adjuvants and additives and their impact on the factors determining the effectiveness of biocontrol agents.
Table 3. Selected adjuvants and additives and their impact on the factors determining the effectiveness of biocontrol agents.
SubstancesDeposition and Aid StickerDrift ControlPenetrantSpreader and WetterChemical Precipitation PreventerAni/DefoamerWeather and UV ProtectionReferences
Organosilicon surfactants+ ++ ++[46,52]
Saponins+ ++ [53,54]
Rhamnolipids+ ++ [55,56]
Mannosylerythritol lipids+ ++ [57,58]
Oils and lipids+++ ++[37,49]
Biopolymers++ + ++[59]
Humus substances+ ++ +[60,61]
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Holka, M.; Kowalska, J. The Potential of Adjuvants Used with Microbiological Control of Insect Pests with Emphasis on Organic Farming. Agriculture 2023, 13, 1659. https://doi.org/10.3390/agriculture13091659

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Holka M, Kowalska J. The Potential of Adjuvants Used with Microbiological Control of Insect Pests with Emphasis on Organic Farming. Agriculture. 2023; 13(9):1659. https://doi.org/10.3390/agriculture13091659

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Holka, Małgorzata, and Jolanta Kowalska. 2023. "The Potential of Adjuvants Used with Microbiological Control of Insect Pests with Emphasis on Organic Farming" Agriculture 13, no. 9: 1659. https://doi.org/10.3390/agriculture13091659

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