Modes of Action of Entomopathogenic Fungi

Abstract

Commercial formulations of entomopathogenic fungi are successfully applied as an alternative to chemical agents in control of agricultural pests. One of the major properties of these species is building resting spores under unfavorable environmental conditions and having facultative or saprophytic properties. Mitosporic fungi such as Beauveria bassiana, Lecanicillium lecanii, Metarhizium anisopliae and Isaria fumosorosea are common species worldwide and capable of infect species from Lepidoptera, Hemiptera, Coleoptera and Diptera. Entomopathogenic fungi infests the host insects via digestion, respiration and through integument. In infestation from integument which is one of the most common infestation methods, fungi grows hyphae to penetrate epicuticle and progresses into hypodermis to achieve the infestation. Anamorphic fungi like B. bassiana and M. anisopliae primarily propagates as blastospores rather than hyphal development and these blastospores invade the vital organs by dispersing across the insect body via circulation of hemolymph within body cavity and eventually result in death of insect by clogging the circulatory system. The fungus moves to facultative feeding phase after death of host and initiates hyphal development outwards the integument, builds massive amount of spores. Conidiospores found on conidiophores are utilized to establish new infestations. Some entomopathogenic fungi are capable of killing the host even faster by excreting some mycotoxins (like beauvericin, cyclodepsipeptide, destruxin and desmethyldestruxin) at earlier stages of the infestations. Toxigenic fungi are able to kill the host earlier as compared to non-toxigenic species. In this study, information on the mechanisms used by entomopathogenic fungi for infestation of their hosts are presented.

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MODES OF ACTION OF ENTOMOPATHOGENIC FUNGI
Hacer Handan Altinok 1,*, Mahmut Alper Altinok 1, Abdurrahman Sami Koca 2
1
Erciyes University, Faculty of Agriculture, Department of Plant Protection,
38039 Kayseri, Turkey
2
Bolu Abant Izzet Baysal University, Faculty of Agricultural and Natural Science,
Department of Plant Protection, Bolu, Turkey
Abstract
Commercial formulations of entomopathogenic fungi are successfully applied as an alternative to chemical agents in
control of agricultural pests. One of the major properties of these species is building resting spores under unfavorable
environmental conditions and having facultative or saprophytic properties. Mitosporic fungi such as Beauveria
bassiana, Lecanicillium lecanii, Metarhizium anisopliae and Isaria fumosorosea are common species worldwide and
capable of infect species from Lepidoptera, Hemiptera, Coleoptera and Diptera. Entomopathogenic fungi infests the
host insects via digestion, respiration and through integument. In infestation from integument which is one of the most
common infestation methods, fungi grows hyphae to penetrate epicuticle and progresses into hypodermis to achieve the
infestation. Anamorphic fungi like B. bassiana and M. anisopliae primarily propagates as blastospores rather than
hyphal development and these blastospores invade the vital organs by dispersing across the insect body via circulation
of hemolymph within body cavity and eventually result in death of insect by clogging the circulatory system. The fungus
moves to facultative feeding phase after death of host and initiates hyphal development outwards the integument, builds
massive amount of spores. Conidiospores found on conidiophores are utilized to establish new infestations. Some
entomopathogenic fungi are capable of killing the host even faster by excreting some mycotoxins (like beauvericin,
cyclodepsipeptide, destruxin and desmethyldestruxin) at earlier stages of the infestations. Toxigenic fungi are able to
kill the host earlier as compared to non-toxigenic species. In this study, information on the mechanisms used by
entomopathogenic fungi for infestation of their hosts are presented.
Keywords:
Biological control, Fungi, Mycoinsecticide, Pest management
1. INTRODUCTION
Entomopathogenic fungi have important roles in the natural regulation of many insect pests and pest
populations. Several species of entomopathogenic fungi are being produced commercially and used
as biological control agents against many insect pests in many parts of the world (Sevim et al.,
2015). The use of pesticides against pests, disease agents and weeds in agricultural lands are
problematic, which causes deterioration of natural balance and environmental pollution. In addition,
it directly and indirectly affects human health negatively (Eken and Demirci, 1997). When all these
issues are considered, the importance of alternative control methods and integrated management
methods draw the attention (Erkılıç and Uygun, 1993).
Integrated and biological control methods emerged as an alternative to chemical control (Bora,
2002). Research on microbial control within biological and integrated control methods has started to
increase (Eken and Demirci, 1997; Milner, 2000; Rumbos and Athanassiou, 2017). Today, many of

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the fumigants used in control of storage pests are either banned or restricted. Entomopathogenic
fungi from Lecanicillium, Isaria and Beauveria genus are reported as effective to adults of storage
pests such as Acanthoscelides obtectus (Ondráčková, 2015). Mostly, biological control is used with
the aid of various organisms or their toxic metabolites to prevent the activity of pests, disease agents
and weeds in cultivated plants (Isaac, 1992). Some entomopathogenic fungi are able to kill the host
even faster by excreting some mycotoxins (like beauvericin, cyclodepsipeptide, destruxin and
desmethyldestruxin) at earlier stages of the infestations. Toxigenic fungi are able to kill the host
earlier as compared to non-toxigenic species (Wang et al., 2018).
Entomopathogens are called as organisms that cause disease in insects. The use of microorganisms
such as fungi, bacteria, viruses, rickettsia and nematodes living on harmful insects to kill them is
known as microbial control (Öncüer, 1995). Entomopathogenic fungi are biological control agents.
They play an important role in suppressing many pest populations (Roy et al., 2006) and used
successfully in many phytophagous Arthropods in nature (epizootic) or in laboratories. Many
studies have been carried out on microbial control using entomopathogenic microorganisms with
biological control methods against these phytophagous species. (Alay, 1965; Zare and Gams, 2001;
Kim, 2007; Demirci et al., 2008; Gurulingappa et al., 2010; Xie et al., 2010). There are more than
500 species of fungi that can infect insects (Roberts, 1981; Hall and Papierok, 1982; Zimmermann,
1986; Erkılıç and Uygun, 1993; Kılıç and Yıldırım, 2008). Entomopathogenic fungi have been
identified in various parts of the world and they create an effective suppression on natural insect
populations (Tanada and Kaya, 1993; McCoy et al., 1988). Some fungi species are used
successfully in the biological control of various pests, disease agents and weeds in the world (Eken
and Demirci, 1997).
The aim of the present review is to summarize infection mechanism of some entomopathogenic
fungi and use of these fungi as mycoinsecticides.
2. ENTOMOPATHOGENIC FUNGI AND THEIR ACTION MECHANISM
The entomopathogenic fungi are used in microbial control to prevent arthropod species in cultivated
lands. These fungi take place in Ascomycota, Basidiomycota, Entomophthoromycotina,
Blastocladiales, Kickxellomycotina, Microsporidia and Neocallimastigomycota subdivisions (Stock
et al., 2009). Table 1 shows some licensed fungus content widely used as microbial insecticides
worldwide (Milner, 2000). Table 2 shows the common fungal insecticides in Turkey.
Table 1. Some common fungus-containing microbial insecticides commonly used worldwide
Fungi species Effective Host Commercial Name
Beauveria bassiana (Bals. Criv) Vuill. Whiteflies, aphids, thrips Mycotrol
B. bassiana Sucking insects Naturalis
Metarhizium anisopliae (Metchnikoff)
Sorokin Termits BioBlast
Lecanicillium lecanii
R. Zare & W. Gams Aphids Vertalec
L. lecanii Whiteflies Mycotal
Paecilomyces fumosoroseus
(Wize) A.H.S.Br & G.Sm. Whiteflies, thrips PFR-97
B. brongniartii Manas larvae Engerlingpilz
M. anisopliae Grasshoppers Green Muscle
B. bassiana Manas larvae Betel

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Table 2. Common fungal insecticide in Turkey
Fungi species Effective Host Commercial Name
Metarhizium anisopliae Whiteflies, thrips, aphids and caterpillars MET52 EC
Metarhizium anisopliae Whiteflies, thrips, aphids and caterpillars MET52 G
Entomopathogenic fungi enter through the cuticle directly (Sevim et al., 2015). This process occurs
partly physically and enzymatically (Erkılıç and Uygun, 1993; Clarkson and Chamley, 1996). The
action mechanisms of entomopathogenic fungi; firstly, the fungus spores settle on the insect cuticle,
then the spores germinate and enter the cuticle by forming appressorium. Hyphae develop in
hypodermis and they continue to multiply in insect body and blood cells and cause the death of the
insect. Permanent sexual and asexual periods occur with asexual spores that can spread by
saprophytic development on these dead individuals (Glare and Milner, 1991).
One of the most studied subjects about entomopathogenic mechanism is toxin secretion of fungi.
For example, Beauveria bassiana and Metarhizium anisopliae secrete toxin in artificial
environments. These substances can cause insect death even before spread and form spores in tissue
of parasitic fungus. In most cases, the digestion of fungal propagules can cause death due to toxic
effect rather than mycosis (Charnley, 2003). One of the most important features of insect is parasitic
fungi forms resistant to environmental conditions and they have saprophytic properties. Therefore,
they can be isolated from soil and organic wastes and increase the chance of using as biological
agents (Erkılıç and Uygun, 1993).
3. INFECTION FORMS ON INSECTS OF ENTOMOPATHOGENIC FUNGUS
Entomopathogenic fungi have wide range of morphologically, phylogenetically, and ecologically
diverse fungal species and exhibit phylogenetic diversity that reproduce via sexual or asexual
spores, or both. Entomopathogenic fungi infect host insects by digestion, respiration, and
particularly through the skin. Mouth parts have great importance in infection by digestion. For
example, while insecticides cannot be infected by artificial infection of Beauveria tenella (Delacr.)
to the intestines of Melolontha melolontha L. larvae, the fungus can be produced by oral control
(Ferron, 1978; Sevim et al., 2015).
It is known that enzymes capable of degrading the chitin-protein composition in insect skin have an
important role in transdermal infection (Clarkson and Chamley, 1996). After the entomopathogenic
fungus spore adheres to the skin of the insect, if the climatic conditions are favorable, it forms the
germination nail and penetrates the epicuticula with the help of oil and protein degrading enzymes
and reaches hypodermis. Then, these hyphae multiply and spread in the body cavity. Micelles
filling the body cavity kill the insect. The fungus forms chlamydospores and keep alive in the dead
insect body. These chlamydospores germinate under appropriate conditions to form conidiophores
on the skin of the dead insect. The spores on conidiophores are also ready for new infections
(Ferron, 1978; Shah and Pell, 2003; Goettel et al., 2005).
The fungus should reach the hypodermis in order to be successful in transdermal infection. This is
very important because of molting in insects. Especially, it gets more important for insects that
molting at frequent and short periods of time. If the insect molt before the fungal infection reaches
to the hypodermis, it can rescue from the infection. But if the infection reaches to the hypodermis,
the insect cannot rescue itself from the infection (Öncüer, 1984).

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Entomopathogenic fungi-based biopesticides including Beauveria bassiana and Metarhizium
anisopliae are the most frequently used entomopathogenic fungi worldwide (Faria and Wraight,
2007).
4. IMPORTANT ENTOMOPATHOGENIC FUNGUS SPECIES
Beauveria bassiana
Beauveria bassiana (Balsamo) Vuillemin (Hypocreales: Cordycipitaceae) is the best known as an
insect pathogen. The teleomorph name has been Cordyceps bassiana. Beauveria bassiana known as
“white muskadin” causes to disease in insects. This fungus produced aerial conidia, single-cell
blastospores by germination when they come into contact with the upper skin layer of insects and
penetrate directly into the bodies of their hosts from the upper skin (Kim et al., 2010). The fungus
proliferates rapidly in the body by producing toxins. Therefore, unlike bacterial and viral pathogens
of insects, just a contact is sufficient for infection of B. bassiana and other fungus pathogens. When
fungus kills its host, it evolves outward by covering the insect with a white layer of mildew. This
mildew produces millions of new infective spores that released into the environment. Beauveria
bassiana is widely distributed in nature and has a potential to control with a broad host range of
approximately 700 insect species used for management of many crop insect pests. This fungus is
applied as conidial sprays against insects. B. bassiana is used as a control agent in the field and
laboratory against a large number of pests such as whiteflies, aphids. In addition, B. bassiana does
not harm a large number of non-target organisms (Irigaray et al., 2003). Entomopathogenic fungi
have a wide host range than the other biological control agents. They are known to infect
Lepidoptera, Hemiptera, Coleoptera and Diptera species, and B. bassiana, M. anisopliae and L.
lecanii are widely used worldwide (Deacon, 1983). One of the most controversial issues about
entomopathogenic fungi is the secretion of toxins from these organisms. It was reported that B.
bassiana was produced locally in China and used against Ostrinia nubilalis and Dendrolimus spp.
(Erkılıç and Uygun, 1993). B. bassiana can be successfully used against Leptinotarsa decemlineata
in Turkey (Çam et al., 2002).
Entomopathogenic fungi and pesticides can be used in integrated pest management (IPM) programs
considering the fungus as an important pest control agent. Beauveria bassiana is easily used
together with other chemical insecticides (Chloronicotiyl, Imidaclorid) and provides a synergistic
effect in control of Bemisia tabaci. However, it should never be used together with commercially
available fungicides (Maneb, Mancozep, Thiophanatemetihyl), because these commercial
fungicides are the chemicals that inhibit the growth of mycelium of B. bassiana (Hoddle, 1999).
Anamorphic fungi such as B. bassiana and M. anisopliae are generally developed as biological
control agents applied together against pest populations. These fungi are less likely to multiply in
the biotic environment and remain in nature during their application. Therefore, studies on these
fungi are related to biopesticide aspects rather than their basic ecology. Anamorphic
entomopathogenic fungi naturally spread extensively, particularly in soil. However, less
information is known about their feeding behavior, population structure, factors affecting their
distribution, and the variation of virulence-related characters (Chandler, 2005).
Metarhizium anisopliae
Metarhizium anisopliae (Metsch) Sorok (Ascomycota: Clavicipitaceae) usually multiply in the form
of blastospores or hyphae structures in their host, similar to yeasticidal and spread to the body
cavity with blood fluid movement in the insect body. M. anisopliae is a mitosporic fungus with
asexual reproduction. The spores of these fungi penetrate into the insect body by contact and kill the

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host. They have cylindrical conidia produced and subcylindrical phialides. The disease caused by
the fungus is known as green muscardine disease because of the green colour of its spores (Driver at
al., 2000). It is a biological agent for use in greenhouses where bumblebees and natural enemies are
present. The effectiveness of M. anisopliae against flower thrips (Frankliniella occidentalis Perg.),
which is an important pest in pepper cultivation, has been investigated and found as effective as the
licensed fungicides (Dura, 2010). Due to the biological origin of contact-effective M. anisopliae, it
has no side effects on both the environment and humans.
Entomopathogenic fungi are able to colonize in plant roots as symptomless endophytes. M.
anisopliae is both entomopathogen and endophyte in soil, insects and they can colonize in roots of a
variety of plants resulting in increased plant growth and tolerance against pests and diseases (Sasan
and Bidochka, 2012).
Lecanicillium lecanii
L. lecanii is an entomopathogenic fungus species, that was previously widely known as Verticillium
lecanii. The spores of the Lecanicillium lecanii germinate and produce hyphae on insects and
penetrate into the body cavity where they rapidly develop tissue destruction. The fungus entering
the insect forms blastospores. Then the fungi invasion on the insect cuticle occurs and destroy the
insects within 7-10 days. Dead insects have white fungal hairs (cottony appearance, ranging from
white to pale yellow). When examined under a microscope, the mycelium of the fungus appears as
bright white strands (Anonymous, 2018a). L. lecanii is the most widely used as a commercial agent.
The limitation factor of the use of these preparations depends on high levels of moisture for a long
time to improve their development and effectiveness. Vertalec and Mycotal are produced from
blastospores of L. lecanii which a preparation in wettable powder (WP) formulation. Today,
Vertalec is used against aphids and Mycotal is used against whiteflies as successfully in
greenhouses in western European countries. It is also stated that some strains of L. lecanii can be
used against thrips and crustaceans in greenhouses (Hall, 1985).
Studies have been carried out for the microbial control of the species in the Hyphomycetes group
due to less problems in production and application of entomopathogenic fungi. As a result of these
studies, preparations containing isolates of some species have reached commercially available
stages (Butt et al., 1999). Entomopathogenic fungi were affected by environmental conditions
during germination and penetration stages after application and limited their usage possibilities.
However, advances in formulation showed that these limitations may also be overcome. Also, shape
design type and setting of application period may be useful to overcome these limitations (Butt et
al., 1999).
Isaria fumosorosea
Isaria fumosorosea is a common entomopathogenic fungus, formerly known as Paecilomyces
fumosoroseus. The blastospores of I. fumosorosea grow when they contact with the upper skin layer
of insects and thrive penetrating directly the bodies of their hosts. They completely cover the body
of the pest, and finally kill the hosts (Anonymous, 2018a). I. fumosorosea has wide tolerance range
of temperature and rapidly develop. I. fumosorosea has been isolated from various insect orders and
soil in many regions of the world (Hummer, 1992; Smith, 1993). It has been reported to spread
rapidly both nature and greenhouse conditions in 48 insect species belonging to nine insect orders.
It was reported that I. fumosorosea caused death of the tobacco whitefly (Bemisia tabaci) in nymph
and adult stage both in field and greenhouses conditions. It also caused death of the greenhouse
whitefly (Trialeurodes vaporariorum) in greenhouse conditions (Lacey et al., 1996).

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The studies show that that I. fumosorosea isolates have the potential in the control of greenhouse
whitefly in tomatoes and the temperature of greenhouse does not restrict the growth of fungi (Gökçe
and Er, 2002).
Purpureocillium lilacinum
P. lilacinum (syn: Paecilomyces lilacinus) has a wide habitat, including cultivated or uncultivated
soils, forests, grasslands and deserts. This species can develop between 8-38°C, while the optimal
temperature is 26-30°C (Anonymous, 2018b). P. lilacinum conidiophores form a dense mycelium.
Spores germinate when there is optimal moisture and nutrients. The vegetative hyphae are 2.5-4.0
microns. Conidiophores are 400-600 microns (Anonymous, 2018b). P. lilacinum was firstly found
on Meloidogyne incognita eggs in Peru. This fungus is a facultative parasite of M. incognita eggs
and it can also infect the other Meloidogyne spp. species (Whitehead, 1998). P. lilacinum infect M.
incognita eggs and reduce larvae emerging from these eggs. Infection occurs on Meloidogyne eggs
by producing enzymes that break down the eggshell by the fungus. Serine protease enzymes
secreted by the fungus causes structural changes in the eggshell of the nematode. About 251 isolates
of P. lilacinum restricted the development of Meloidogyne javanica eggs. Thus, the number of
larvae hatched decreased and a large part of larvae hatched died (Whitehead, 1998).
5. CONCLUSIONS
Chemical control is more prominent to protect against harmful insects in agricultural areas. There
are many side effects of chemical control, increasing environmental toxicity and resistance to pest.
In addition, chemicals cause damage to beneficial organisms, causing a loss of natural balance. In
this review, entomopathogenic fungi and other studies about the issue were compiled as alternative
to chemical control, environmentally friendly and not disturbing the natural balance. However, it
was seen that the studies on this issue are not sufficient in Turkey. These studies should be
increased and the use of entomopathogenic fungi in the practice of biopreparation should be
expanded in Turkey. The information presented in this review will be the source of the studies
about entomopathogens in Turkey.
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