The loss in productivity due to crop damage from insects represents a serious threat to the agricultural sector. The global crop loss due to insects contributed to losses of almost $470 billion each year (Culliney 2014), with the global expenditures on pesticides being in the range of $56 billion in 2012. Strikingly, of the $56 billion, only $2–3 billion was spent on biopesticides (Marrone 2014). In the USA, insecticides contributed to almost 14% of all pesticide expenditures (Sabarwal et al. 2018).
The most common strategy for controlling insect invasions is the use of synthetic chemical pesticides, such as Chlorpyrifos, Acephate and Bifenthrin (Dai et al. 2019a). However, insecticidal resistance has become an undeniable phenomenon, and has led to the disastrous collapse of the pest control in many countries (Naqqash et al. 2016). There are also other concerns arising regarding the use of these synthetic chemicals, namely with food safety, adverse effects to non-target organisms—especially those beneficial antagonists of insects—and the environmental impact associated with the use of harmful chemical compounds (Sandhu et al. 2017). The drawbacks to conventional insecticides spurred the search for potent and ecofriendly biocontrol agents.
Biological control agents offer more advantages than their chemical counterparts, since they are safe for other non-target organisms and infect only specific species, with long-term results on target pests (Sanda and Sunusi 2016).
In particular, the entomopathogenic fungi, have the capacity to reduce or eradicate insect populations. Most fungi used for the control of insect pests are ascomycetes, which are usually found in the soil and can cause natural outbreaks on their own when environmental conditions are favorable. Some fungal strains have been developed into commercial products because of their ability to be mass produced (e.g. Beauveria bassiana, Lecanicillium muscarium, Metarhizium anisopliae). These can infect a widerange of insect hosts. Specific fungal strains in commercial products target insect groups such as Coleoptera, Diptera, Hemiptera, Hymenoptera, Lepidoptera and Orthoptera (Dauda et al. 2018).
Some entomopathogenic fungi can also exist as plant endophytes in a variety of hosts. They can exhibit dual functions, acting against insects and plant pathogens, thus giving protection to plant hosts. Moreover, they can have additional roles in endophytism, plant disease antagonism, growth promotion and rhizosphere colonization (Yun et al. 2017; Jaber and Ownley 2018).
Generally, the first mode of action of entomopathogenic fungi is to produce sticky spores to insure adhesion to the body of the host. The non-specific adhesion mechanism of the conidia is due to their hydrophobic properties, which has protein interactions with the hydrophobic exoskeleton of the susceptible host. The spores germinate quickly and initiate penetration of the insect exoskeleton. The fungal cells multiply in the hemocoel of the host’s body, increasing the turgor pressure and eventually killing the insect. The entomopathogen grows in the host’s cadaver to optimize spore production and dispersal under favorable environmental conditions (Roy et al. 2006). High numbers of spores are required to insure infection, with a minimum of 19108 to 19109 conidia/ml (Inglis et al. 2012).
Entomopathogenic fungi also produce secondary metabolites that can act as toxins with insecticidal effects. Proliferating protoplasts produce these compounds to weaken the host’s defense mechanisms, causing rapid death (Hussain et al. 2014). The entomopathogens that produce toxins are more effective at killing the insect hosts as compared with those strains that do not produce such metabolites (Kershaw et al. 1999). There are a variety of active compounds produced by entomopathogenic fungi that exhibit insecticidal properties. Beauvericin is a well-known active compound produced by entomopathogenic fungi. It plays a key role in the virulence of fungi that infect arthropods (Rohlfs and Churchill 2011). It is a cyclic hexadepsipeptide, containing three D-hydroxyisovaleryl and three N-methylphenylalanyl residues in alternating sequence, and belongs to the enniatin antibiotic family. It is structurally similar to enniatins; however, it differs in the nature of its N-methylamino acid (Wang and Xu 2012). It was first isolated from Beauveria bassiana (Hamill et al. 1969) and later from Fusarium species (Liuzzi et al. 2017). Beauvericin has a strong insecticidal function against a broad spectrum of insects. Since the target insects are moving organisms, the entomopathogenic fungi producing beauvericin are more effective insecticidal agents than the direct use of the compound. Beauvericin was first discovered to have insecticidal activity by Hamill et al. (1969). Other studies proved the efficacy of beauvericin in killing other insects, such as Calliphora erythrocephala, Lygus spp. (Leland et al. 2005), Aedes aegyptii (Grove and Pople 1980), Spodoptera frugiperda and Schizaphis graminum (Ganassi et al. 2002); however, it can also be toxic to bees, thus posing a threat to other beneficial insects when applied in the field. Bassianolide (37) a cyclic depsipeptide from Lecanicilium lecanii, exhibits moderate cytotoxicity and an immunosuppressive effect to insect hosts. It can cause significant maximum mortality to Plutella xylostella at 0.5 mg/ml concentrations (Keppanan et al. 2018). As in other groups of fungal cyclopeptides, several variants if bassianolies are known (Matsuda et al. 2004).
Destruxins (38–40), the cyclic hexadepsipeptide mycotoxins are produced by Metarhizium anisopliae. They can kill a variety of insect pests. The purified destruxins can cause toxic effects on the larval developmental stage of mosquitoes (Aedes aegyptii) with high mortality rates (Ravindran et al. 2016). The study of Dong et al. (2016) also revealed positive correlations between destruxin production and blastospore formation, and the producer strain
has the potential to be developed into a mycoinsecticide. Enniatins (41–44) are only produced by Fusarium species. They act as ionophores that bind with ammonium in the transport of ions in the lipid bilayer membrane of the cell. This ionophoric property of enniatins leads to the toxic action in the cell through the disturbance of the normal physiological concentration. Their best studied derivative, Enniatin B was previously shown to exhibit insecticidal activity against blowfly (Calliphora erythrocephala) and mosquito larvae (Aedes aegypti) (Grove and Pople 1980).
The successful application of entomopathogenic fungal strains relies on several factors, such as level of virulence, production efficiency and level of safety to humans and other non-target species. Virulence depends on a complex of factors, such as spore hydrophobicity, which is involved in the conidial adhesion, germination polarity of the spores wherein unidirectional spores are more virulent than multi-directional ones, presence of hydrolytic enzymes to breach the host’s defense wall, and sensitivity to abiotic factors like temperature and humidity. Moreover, entomopathogenic fungi should only be considered for commercialization if they demonstrate high production efficiency, wherein the strains have minimum requirements for growth and can be grown and mass produced in solid substrate (Hussain et al. 2014), thus reducing production costs.
Certain techniques should be considered in order to increase the effectiveness of mycoinsecticides. Since insect larvae usually embed themselves into plant tissues or soil and do not feed on crops (Hall 1998), they do not typically stay in a specific location and therefore are very difficult to target. Spray application can be inefficient at this stage and depositing mycoinsectides over a field or crop may not be effective. Therefore, granular formulations which coat dry spores onto bran or grains, or the drying and fragmentation of mycelium to hold spores in starch, can both be effective methods to treat insects in the field (Hall 1998). Adding the granular substances to mycoinsecticides increases the accuracy and efficiency of the spray.
Several tactics have been identified by Lacey and Kaya (2007) to increase the effectiveness of mycoinsecticides. Preventive applications could be inefficient because the residues are not long-lasting, and therefore they should be applied only when the target pest is seen. Mycoinsecticides should be applied before the pest population reaches peak numbers, and therefore early application is essential. Timing is also important: identifying the life cycle of the host, which has a higher probability of being in contact with the spores, could also increase the effectiveness of the mycoinsecticide. For example, Beauveria bassiana is more efficient in infecting active nymphs than winged adults. Moreover, mycoinsecticides should not be applied during droughts because the environmental conditions are not favorable for the germination of the spores.
Approximately 750 fungal species have been identified as insect pathogens; however, in 1998 only 12 species were utilized as mycoinsecticides in insect sprays (Wraight and Carruthers 1998). By 2007 the number of mycoinsecticides had increased to about 110 commercially available products in the market (de Faria and Wraight 2007). The number has continued to increase, with almost 2700 arthropod pesticides introduced worldwide (Cock et al. 2010), in which about 230 species of biological control agents have been marketed and available for commercial use (van Lenteren 2012). The demand and commercial application of microbial pesticides have increased tremendously. Of 82 microbial biopesticides registered in Brazil, nearly 46% are mycoinsecticides (Mascarin et al. 2018). Fungal biopesticides contributed to a large portion of this increased demand and popularity in pest management in the past two decades (Jaronski and Mascarin 2017). Several products have already disappeared from the international marketplace because they were not commerically successful, but a substantial number of fungal species have been exploited (Kabaluk et al. 2010; Lacey et al. 2015).
De Faria and Wraight (2007) and Mascarin et al. (2018) listed representatives of mycoinsecticides derived from Beauveria, Isaria, Lecanicillium, and Metarhizium species found in the market. Most developed mycoinsecticdes were made for European and American markets, whereas only a few were aimed at the African and Asian markets.
There have been continual obstacles and challenges to the development and commercialization of fungal biological control agents for use in controlling insect populations, ranging from gaps in understanding the basic biological knowledge to their potential socio-economic impact. Problems regarding the effectiveness of insecticides are linked to economic production. The increase in pest-resistance to chemical formulas has led to drastic environmental problems. New chemical insecticides are not being developed quickly enough, and therefore there is room for microbial insecticides, which are growing at the rapid pace of 10–25% per year (Starnes et al. 1993), within the market. Enhancing the virulence of potential fungal species is essential for mycoinsecticides to develop and reach their market potential.
The future of mycoinsecticides is promising, with continued research to increase pathogenic virulence of entomopathogenic fungi in order to achieve commercial success with genetic and physiological engineering. Further studies should be conducted to determine the fungal traits responsible for the effectiveness of mycoinsecticides, enhancement of their virulence, and development of ecofriendly and effective pest management strategies.