ISSN: 2321-3485
Impact Factor : 2.5230[UIF-2015]
Volume - 3 | Issue - 40 | 1st Feb- 2016
Reviews Of Progress
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AGROBENEFICIAL ENTOMOPATHOGENIC FUNGI – Beauveria
bassiana: A REVIEW
1
P. Saranraj1 and S. Sivasakthi2
Assistant Professor of Microbiology, Department of Biochemistry, Sacred Heart
College (Autonomous), Tirupattur, Tamil Nadu, India.
2
Department of Microbiology, Annamalai University, Annamalai Nagar,
Chidambaram, Tamil Nadu, India.
ABSTRACT
The use of microorganisms for the biological control of pest and disease vector
insects was firstly proposed in the midst of the 19th century, however only recently the
full potential and the many advantages of this practice reached application on a
commercial scale. While, only a small percentage of arthropods are classified as pest
species, they nevertheless cause major devastation of crops, destroying around 18% of
the world annual crop production, contributing to the loss of nearly 20% of stored food
grains and causing around US$100 billion damage each year. The entomopathogenic
fungus Beauveria bassiana is a globally distributed Hyphomycete, strains of which infect
a range of insects. Strains of Beauveria
bassiana have been used as the active
agents in a number of biopesticides against
a variety of agricultural pests, including
whiteflies, beetles, grasshoppers and
psyllids. The fungus is a facultative
saprophyte and there are reports of
Beauveria bassiana growing as a plant
endophyte and interacting with plant roots.
In this present review, we discussed about
the general characteristics of Beauveria
bassiana, History of Beauveria bassiana, Morphological, cultural & molecular
characteristics of Beauveria bassiana, Life cycle of Beauveria bassiana, Factors
responsible for germination of conidia of Beauveria bassiana, Growth characteristics of
Beauveria bassiana, Pathogenicity of Beauveria bassiana, Biocontrol properties of
Beauveria bassiana, Solid and diphasic production technologies, Blastospore production
of Beauveria bassiana, Formulations of Beauveria bassiana and Agricultural importance
of Beauveria bassiana.
Key words: Entomopathogenic fungi, Beauveria bassiana, Blastospores, Formulation,
Insect pests, Agricultural crops and Biocontrol.
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1. INTRODUCTION
Insecticides are the only tool in the pest management strategy that is reliable for
emergency action when insects at the times of blooming. However, insecticidal control
has led to several problems in insect management such as appearance of insecticide
resistance pests, pest resurgence, undesirable toxic effects to natural enemies of target
pests, disruption of the ecosystem, toxic residues in crop plants and environmental
problems. Consequently, the research for new environmentally safe method is being
intensified.
The indiscriminate use of synthetic pesticides causes some unfortunate
consequences such as environmental pollution, pest resistance and toxicity to other non target organisms including human being. At present scenario biopesticides are considered
as the best alternative to chemical pesticides in the integrated pest management
programmed. Current estimates indicate that the global annual market for pesticides for
which there may be biological alternatives. To date, however, only a relatively minor
portion of this market has been captured by biological agents, most of which are the
various forms of Bacillus thuringiensis. With respect to mycoinsecticides, intensive
research over the past several decades has elevated most of the concerns regarding these
agents, such as stability, formulation and application, mass production, and toxicity to
non target pests. Field trials have proven that fungal applications can effectively reduce
target insect populations, in this case grasshoppers, within a relatively short period of
time.
Biological control agents such as entomopathogenic fungi (EPF) can be used as a
component of integrated pest management (IPM) of many insect pests. Under natural
conditions, these pathogens are a frequent and often cause natural mortalities of insect
populations. The main drivers behind the push for mycoinsecticides are the need for more
specific agents as components of IPM programmes due to concerns over chemical
residues on human health and the environment.
Microbial assemblages in agricultural soils are important for ecosystem services
in sustainable agricultural systems, including pest control. High populations of beneficial
soil borne organisms are characteristics of healthy soils. The soil environment constitutes
an important reservoir for a diversity of entomopathogenic fungi, which can contribute
significantly to the regulation of insect populations. Many species belonging to
Hypocreales (Ascomycota) inhabit the soil for a significant part of their life cycle at
northern latitudes. Of these, Beauveria bassiana are especially common (Keller et al.,
2013). Conversion from conventional to organic farming generally increases the diversity
and activity of soil microorganisms over time (Mader et al., 2012). There is evidence for
higher population levels of entomopathogenic fungi in soils of organically farmed fields
as opposed to conventionally farmed fields (Klingen et al., 2012).
Entomopathogenic fungi have played a uniquely important role in the history of
microbial control of insects. Historical evidence indicated that entomopathogenic fungi
were the first to be recognized as disease causing microorganisms in insects. Agostino
Bassi wrote about a disease in silkworm caused by a fungus, which was later, identified
as Beauveria bassiana (Kikankie, 2009). Elie Metchnikoff began with study of disease of
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a grain beetle Anisoplia austriaca that resulted in the discovery of the fungus
Metarhizium anisopliae (Zimmermann, 2007). Beauveria bassiana, commonly known as
white muscardine fungus attacks a wide range of immature and adult insects.
Metarhizium anisopliae a green muscardine fungus is reported to infect 200 species of
insects and arthropods. Both of these entomopathogenic fungi are soil borne and widely
distributed.
The entomopathogenic fungus Beauveria bassiana is well known as a potential
alternative to chemical pesticides for the control of insect pests and is commercially
available for such purposes in numerous countries worldwide. As a broad host range
insect pathogen, strains of this fungus have been exploited for use against crop and
invasive pests as well as for insects that act as human and animal disease vectors such as
mosquitoes and ticks (De Faria and Wraight, 2007; Farenhorst, 2009; Kirkland et al.,
2014). Aside from its interest as a pest biological control agent, Beauveria bassiana is
also an emerging model organism that can be used to examine unique aspects of fungal
growth and development including host pathogen interactions (Lewis, 2009; Wanchoo,
2009; Jin, 2010). Infection of insects does not require any specialized mode of entry and
begins with attachment of fungal spores to the target hosts. In response to cuticle surface
cues, the fungus germinates, and the emerging germ tubes produce a variety of enzymes
that combined with mechanical pressure begin the process of cuticle penetration. In this
regards, the surface characteristics of the infectious fungal spores as well as several
genetic determinants of virulence have been characterized (Holder, 2007; Fang, 2008;
Fang, 2009; Holder and Keyhani, 2015).
The entomopathogenic fungus, Beauveria bassiana is of commercial importance
as an alternative to chemical insecticides in an agro ecosystem (Khachatourians et al.,
2012). The fungal pathogen Beauveria bassiana is a widely used mycoinsecticide for
control of several insect pests, providing a biological alternative to synthetic chemical
insecticides (Hajek et al., 2001). A key advantage for microbial control agents is their
potential to replicate and persist in the environment, offering continued suppression of
insect pest populations. Exploiting this advantage, however, is commensurate with the
need to determine the risks to non - target organisms of mass releasing this fungus. To
date, no information is available on the potential for genetic recombination between
strains of Beauveria bassiana neither in agricultural fields nor on whether this
recombination could result in altered virulence and host range.
Beauveria species attack many insect species worldwide. Species range from the
ubiquitous insect pathogen Beauveria bassiana (Balsamo) Vuillemin to rare species but
the entomogenous life - style is prevalent (Glare et al., 2008; Sevim et al., 2010; Glare,
2014). Currently, six species of this genus are recognized: Beauveria bassiana, Beauveria
clade, Beauveria brongniartii, Beauveria caledonica, Beauveria vermiconia and
Beauveria amorpha (Rehner and Buckley, 2015; Goettel et al., 2015). Among these
species, considerable effort has been spent to develop Beauveria bassiana as a biological
control agent in agriculture and forestry in temperate regions and the most widely used
species available commercially was Beauveria bassiana (Meyling and Eilenberg, 2007).
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Although, a sexual stage is now known (Li et al., 2001) most Beauveria bassiana
exist as asexual organisms, reproducing mainly through the production of single cell
conidia. Beauveria bassiana produce three single cell forms, aerial conidia, in vitro
blastospores and submerged conidia in different conditions (Jeffs et al., 2009). Aerial
conidia are produced on the surface of solid medium by a process of hyphal extension,
formation of phialides (rachis) and spore production. Aerial conidia usually are used for
biological control agents because they are relatively resistant to varying environmental
conditions and can be formulated to prolong shelf life. Aerial conidia contain a rodlet
layer that results in a hydrophobic property. Blastospores are produced in nutrient liquid
medium. They are hydrophilic, and they germinate and grow at much higher rate than
aerial conidia. Submerged conidia are produced in defined liquid medium. They are also
hydrophilic, showing a rough surface morphology. Submerged conidia represent an
important developmental stage for growth in a limited nutrient medium (Holder and
Keyhani, 2015).
Entomopathogens can be mass produced using the diphasic liquid – solid
fermentation technique developed for the LUBILOSA (Lutte Biologique contre les
Locustes et Sauteriaux) project to produce Beauveria bassiana (Lomer et al., 2007). The
liquid phase provides active growing mycelia and blastospores, while the solid phase
provides support for development of the dry aerial conidia. The conidia produced by
these fungi can be used directly as natural granules or extracted through sieving and
formulated as powder, granules or oil concentrate, or any other suitable formulation
depending on the target insect pest for example, Beauveria bassiana was applied as
conidia or mycelia in various formulations. Control of insect pests in field after initial
application is achieved through the induction of a fungal epizootic, where new spores,
and vegetative cells produced in infective insects are spread, naturally, to healthy
members of the insect population.
2. BEAUVERIA BASSIANA
The genus Beauveria contains at least 49 species of which approximately 22 are
considered pathogenic (Kikankie, 2009). Beauveria bassiana, a white muscardine fungus,
is the most historically important of the commonly used fungi in this genus. Originally
known as Tritirachium shiotae, this fungus was renamed after the Italian lawyer and
scientist Agostino Bassi who first implicated it as the causative agent of a white (later
yellowish or occasionally reddish) muscardine disease in domestic silkworms (Furlong
and Pell, 2005; Zimmermann, 2007).
All fungal phyla include species that are able to reproduce either sexually or
asexually. The production of multiple spore types increases the chances of survival
during adverse environmental conditions (Alexopoulos et al., 1996). These spore types
can be produced in response to environmental conditions, as well as at different times in
the life cycle and can have different dispersal mechanisms. Beauveria bassiana is
considered to be one of the most effective entomopathogenic fungi for various reasons
including: cosmopolitan distribution (Bidochka et al., 2000), ability to infect any life
stage of its host, wider host range than the other Deuteromycetes, can infect almost all
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orders of insects (Roberts and Hajek, 2002) and can infect certain plant tissues (Bing and
Lewis, 1992). Beauveria bassiana can easily be isolated from insect cadavers or from soil
in forested areas by using simple media (Beilharz et al., 2002), as well as by baiting soil
with insects (Zimmermann, 2006). In the laboratory it can be cultured on simple media
(Goettel and Inglis 2007).
Huang et al. (2002) identified Cordyceps bassiana as the ascomycote teleomorph
of Beauveria bassiana. However, the organism was most frequently described and
identified in the anamorph stage and assigned to the Deuteromycota. Taxonomical
identification within the Deuteromycota relies heavily on physical characteristics such as
shape, size and color as well as the manner in which the asexual spores, or conidia are
produced.
Species within the genus Beauveria are typically differentiated from other fungi
by morphological characteristics. They are filamentous fungi that produce colorless
(hyaline) aerial conidia from conidiogenous cells freely on the mycelia. This
characteristic places them within the moniliaceous (having hyaline conidia)
Hyphomycetes (De Hoog, 1972). Aerial conidia are initially produced as terminal
swellings formed on the neck of the conidiophore. The next conidium grows laterally,
half way up the first neck of the conidiophore, in another direction, and is pushed
upwards by sympodial growth (De Hoog, 1972). The resulting denticulate rachis, with
denticles equally wide as the rachis, is characteristic of Beauveria spp.
Beauveria bassiana colonies grow relatively slowly and can appear powdery or
wooly, with colors ranging from white to yellow and occasionally pinkish. Aerial hyphae
are septate, smooth, hyaline and about 2 µm wide. Submerged hyphae are similarly
structured, but larger (1.5 – 3 µm). Conidiogenous cells, which arise from short swollen
stalk cells, are often found in dense clusters or whorls. They consist of a globose base and
the characteristic denticulate rachis. The aerial conidia are hyaline, smooth, relatively thin
walled and vary from being oval to spherical depending on the species and occasionally
by cultural conditions (De Hoog, 1972; Huang et al., 2002).
Typical of hyphomycete entomopathogens, Beauveria bassiana invades through
the host cuticle, although as with other hyphomycetes, entry through the digestive tract is
also possible. The initial and crucial steps in the infection process are attachment to, and
penetration of, the host cuticle. Arthropod cuticles are complex structures, which in the
case of insects are composed of two main layers the epicuticle and the procuticle (Huang
et al., 2002).
The epicuticle, a thin layer which overlays the procuticle, lacks chitin, but was
composed of sklerotinized proteins overlaid by a waxy layer containing fatty acids,
sterols and lipids. The bulk of the cuticle, the procuticle, consists of chitin embedded in a
protein matrix (Clarkson and Charnley, 1996; Goettel and Inglis, 2007). Fungal
entomopathogens use mechanical pressure and a mixture of enzymes to penetrate and
dissolve the insect cuticle. Although, several entomopathogens use swellings at the tip of
the germ tube (appressoria) to generate mechanical pressure and increase attachment to
the insect cuticle, such structures are rarely observed in Beauveria bassiana. However,
the battery of enzymes including proteases and chitinases produced by this
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entomopathogen are similar in nature to those produced by other hyphomycete
entomopathogens such as Metharhizium ansiopliae (Clarkson and Charnley, 1996).
Once the fungal hyphae reach the hemocoel, thin walled, yeast like, hyphal bodies, or blastospores, are generated and dispersed throughout the host (Goettel and
Inglis, 2007). Host death appears to result from a number of factors including production
of toxins by the fungus, physical obstruction of the circulatory system, invasion of organs
and nutrient depletion. Upon host death, the parasite switches from yeast like to hyphal
growth invading all the tissues of the host body, while attempting to reduce or eliminate
competing organisms with a variety of antimicrobial metabolites. The mummified corpse
can remain in the environment unchanged for months, but under favorable conditions the
hyphae emerge from within the corpse, sporulate and the resulting aerial conidia are
dispersed via, air or water (Goettel and Inglis, 2007).
Beauveria sp. produces a number of metabolites some of which have cytotoxic
effects alexopoulos (Alexopoulos et al., 1996). These metabolites include beauvericin,
bassianolide, beauveriolides, bassianin, tenellin and oosporein. Beauvericin and
bassioanolide are ionophores that differ in specificity for cations. Beauvericin, a
hexadepsipeptide, has antimicrobial activity against both Gram negative and Gram
positive bacteria is toxic to brine shrimp with a LD50 of 2.8 µg ml-1 water, but has no
demonstrated insecticidal effects (Strasser et al., 2000). Bassianolide, a cyclooctadepsipeptide, also has antimicrobial effects and was lethal to silk worm larvae at a
concentration of 13 ppm (Strasser et al., 2000).
Although, beauveriolides are structurally related to beauvericin and bassioanolide,
they are not as well characterized, and their antimicrobial or insecticidal potential have
yet to be described. Strasser et al. (2000) have recently shown that beauveriolides have an
inhibitory effect on lipid drop formation in mouse erythrocytes and as a result could be
marketed as anti-cholesterol drugs. According to their data, beauveriolides have few
cytotoxic effects on mouse cells at levels up to 100 mg-1 day-1. The pigments, bassianin,
tenellin and oosporein are toxic to erythrocyte membrane ATPases (Jeffs and
Khachatourians, 2007). Oosporein is also a denaturing agent and a potent antibiotic
specific to Gram positive organisms. The toxicity of these pigments towards insect host
cells has not been well defined (Strasser et al., 2000).
3. HISTORY OF ENTOMOPATHOGENIC FUNGI Beauveria bassiana
In the early 1800s, the silkworm farms of Italy and France were plagued with
diseases that periodically decimated the European silk industry. The disease was called
white muscardine after the French word for bonbons, as the disease resulted in fluffy
white corpses resembling pastries. An Italian scientist named Agostino Bassi discovered
that the disease was caused by a microbial infection and that it could be controlled by
altering the living conditions of the silkworms to decrease the spread of the disease. One
simple recommendation that he made was to remove and destroy infected and dead
insects. Later the microbe, a filamentous fungus, responsible for the disease was named
Beauveria bassiana in honor of Bassi’s discovery. In 1835 Agostino Bassi, one of the
founding fathers of insect pathology, published his findings in a paper entitled Del mal
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Del segno, calcinaccio o moscardino; this publication was one of the first instance of a
microbe identified as the causative agent of an infectious disease (Alexopoulos, 1996).
The earliest reports of a fungal entomopathogen, possibly the organism that would
come to be known as Beauveria bassiana (Balsamo) Vuillemin, came from China, as far
back as 2700 BC (Steinhaus, 1956). It was not until 1835 that Agostino Bassi
demonstrated that Calcino, or White Muscardine, a disease that was devastating the
Italian silkworm industry, was contagious and caused by a parasitic fungus (Steinhaus,
1956). Balsamo Crivelli officially named the organism Botrytis paradoxica, eventually
changing the name to Botrytis bassiana to honor the man who first described it.
In 1912, Vuillemin, determined that there were enough features peculiar to
Botrytis bassiana to assign it to the new genus Beauveria (De Hoog, 1972). There now
are multiple species in the genus Beauveria Vuill. Some of the most important ones are:
Beauveria bassiana, Beauveria brongniartii, Beauveria alba, Beauveria bassiana and
Beauveria brogniartii well known entomopathogens with a wide host range, including
arthropods other than insects, are now being used as biological control agents to control a
variety of crop damaging insects. Beauveria alba is mainly isolated as an indoor
contaminant and displays the lowest pathogenicity of these three Beauveria species
(Alexopoulos et al., 1996). Due to the practical applications of fungal entomopathogens
as biological control agents, the biology of these fungi has been the subject of much
research.
Agostino Bassi (1835) first described Beauveria as the causal agent of mal del
segno or the mark disease, also known as calcinaccio or cannellino in Italy and white
muscardino in France, which caused economically devastating epizootics of domestic
larval silkworms in southern Europe during the 18th and 19th centuries. In his studies with
Beauveria, Bassi was the first to demonstrate that microbes can act as contagious
pathogens of animals, providing an important antecedent to the germ theory of disease
(Ainsworth, 1973). The first taxonomic recognition of the muscardino fungus was
proposed by Balsamo Crivelli (1835) who acknowledged Bassi’s discoveries by naming
this pathogen Botrytis bassiana. The genus Beauveria, however, was not formally
described until the early 20th century by Vuillemin (1912), who designated Botrytis
bassiana as the type species.
Beauveria bassiana is considered non-pathogenic to vertebrates; although there
are a handful of recorded cases of human infection by this fungus (Kisla et al., 2010;
Tucker et al., 2014). These cases however, involved patients with compromised immune
systems increasing their susceptibility to a wide range of opportunistic infections. Based
upon safety tests and considered a “natural product,” Beauveria bassiana has been
approved by the U.S. Environmental Protection Agency for commercial use. Beauveria
bassiana is non toxic to mammals, birds, or plants; and use of Beauveria is not expected
to have deleterious effects on human health or the environment (EPA, 2000). Strains and
various formulations of Beauveria bassiana are available commercially in various parts
of the world.
Major efforts have been targeted towards isolation and characterization of strains
with high virulence, improved cost effectiveness and to technologies that could be
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applied to other economically important Ascomycetes. One of the most important steps in
the host pathogen interaction is the initial attachment of the fungus to the host cuticle.
Modifying the formulation of commercial products, or of the fungus itself, namely to
improve targeting and attachment to the host cuticle, may lead to improvements in
infection rates and host mortality, and hence the effectiveness of the biocontrol.
Birth of insect pathology occurred in the nineteenth century when the Italian
scientist Agostino Bassi (1835) discovered that disease in silkworm could be caused by a
fungus, which was later identified as Beauveria bassiana (Gillespie and Claydon, 2009).
Ignoffo and Anderson (2009) elucidated the etiology of a contagious disease for the first
time, but also implied that infectious diseases identified as Beauveria bassiana could be
used to control insects. The disease caused by Beauveria bassiana is known as White
Muscardine. This name was derived from a type of cookies produced in Italy, which are
fully covered with sugar giving a whitish appearance.
The insect pests that can be controlled by Beauveria bassiana includes Rice Leaf
folder, Stem borer, Homed cater pillar, Coconut rhinoceros beetle, Brinjal fruit borer,
Colorado potato beetle, May beetle, Whitefly, Aphids, Thrips, Mealy bugs, Psyllids,
Weevils, Caterpillars and Leafhoppers. It was being realized that this fungus was rather a
generalist, with no strict host specificity (Shimuza, 2004).
4. MORPHOLOGY, CULTURAL CHARACTERISTICS AND MOLECULAR
CHARACTERIZATION OF Beauveria bassiana
Beauveria is characterized morphologically by its sympodial to whorled clusters
of short-globose to flask-shaped conidiogenous cells, which give rise to a succession of
one-celled, hyaline, holoblastic conidia that are borne on a progressively elongating
sympodial rachis. Although morphologically distinctive as a genus, species identification
in Beauveria is difficult because of its structural simplicity and the lack of distinctive
phenotypic variation. Conidia are the principal morphological feature used for species
identification in Beauveria. In shape conidia may be globose, ellipsoidal, reniform to
cylindrical, or comma shaped and range in size from 1.7 to 5.5 mm. Species identification
in Beauveria has been complicated by the proliferation of new species described between
the late 19th to mid-20th centuries, few of which are morphologically distinct from
previously described species (Petch, 2006).
Several revisionary studies of Beauveria have been conducted to evaluate
morphological species concepts. Petch (2006) recognized two species, Beauveria
bassiana and Beauveria densa (Link) F. Picard and concluded that cultural data were
uninformative for delimiting species. Macleod (2014) monographed Beauveria and, like
Petch, recognized only two species, which he classified in Beauveria bassiana and
Beauveria brongniartii (Sacc.) Petch (5 Beauveria densa). Macleod (2014) concurred
recognized an additional species, Beauveria alba (Limber) Saccas, which was later
transferred to Engyodontium (Limber) (Hoog, 2008). Hoog and Rao (2015) described
several new species. In all, forty nine species have been placed in Beauveria and 22
epithets are currently valid. Today, researchers generally follow Macleod (2014) and
Hoog (2012) and classify most environmental isolates of Beauveria in either Beauveria
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bassiana or Beauveria brongniartii, a practice reflected in contemporary texts and keys
to species identification (Humber, 2007; Tanada and Kaya, 2013).
Ongoing difficulties in applying morphological approaches to species recognition
in Beauveria have spurred the search for additional sources of taxonomic characters.
Alternative character systems that have been investigated include isozymes (Maurer et
al., 2007), chemotaxonomic characters (Mugnai et al., 2009), mitochondrial RFLP
(Hegedus and Khachatourians, 2006), immunological approaches (Tan and
Ekramoddoullah, 2011), rRNA sequencing (Rakotonirainy et al., 2011), RFLP (Kosir et
al., 2011), introns in the large subunit rDNA (Neuveglise et al., 2006; Neuveglise and
Brygoo, 2014), RFLP and nucleotide sequences of ITS (Neuveglise et al., 2014), SSCP
analysis of taxon specific markers (Hegedus and Khachatourians, 2006), RAPD markers
(Cravanzola et al., 2007; Maurer et al., 2007), and the combined use of morphology and
RAPD markers (Glare and Inwood, 2008). Although, all character systems investigated in
these studies were effective in detecting genetic variation within Beauveria, none have
been applied directly to taxonomic investigations in this genus.
Although, biologically relevant species concepts and explicit species recognition
criteria have yet to be defined for Beauveria, recent molecular and cultural studies have
provided insight regarding the phylogenetic position and reproductive biology of several
species. An rDNA phylogeny by Sung et al. (2001) supports a single evolutionary origin
of Beauveria within the sub-family Cordycipitoideae of the Clavicipitaceae, and that the
teleomorph Cordyceps scarabaeicola is nested within Beauveria and is the sister to
Beauveria caledonica Bissett & Widden. Second, strains isolated from stromata of
several Cordyceps species produce Beauveria anamorphs, clearly demonstrating that
some Beauveria species are sexual. These Cordyceps species include Cordyceps bassiana
(Li et al., 2001), Cordyceps brongniartii (Shimazu et al., 2008), Cordyceps
staphylinidaecola (Kobayasi and Shimazu, 2002) and Cordyceps sobolifera (Li et al.,
2001).
Beauveria is ubiquitous in plant debris and soil and may be isolated from
foodstuffs, infected insects and indoor air environment. It has a wide host range of insects
and is common in nature. Beauveria densa isolated from cadavers was able to attack
Coleoptera and Lepidoptera but not Orthoptera. Beauveria bassiana is the most common
parasite of insects that has been isolated from soil and litter and from dead and moribund
insects in nature. Over 200 species of insects in nine orders, mainly Lepidoptera and
Coleoptera, have been recorded as hosts of Beauveria bassiana. Other Beauveria species,
like Beauveria brongniarti, have been used in France for control of insect pests (Feng et
al., 2004). Beauveria was isolated from insects belonging to the Scarabaeidae family
(Humber, 2007). Beauveria amorpha was recorded in South America from Lepidoptera
and Coleoptera insects (Boucias and Pendland, 2008).
In culture, Beauveria bassiana grows as a white mold. On most common cultural
media, it produces many dry, powdery conidia in distinctive white spore balls. Each spore
ball was composed of a cluster of conidiogenous cells. The conidiogenous cells of
Beauveria bassiana are short and ovoid, and terminate in a narrow apical extension called
a rachis. The rachis elongates after each conidium was produced, resulting in a long zig -
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zag extension. The conidia are single -celled, haploid and hydrophobic. Beauveria
bassiana was usually found growing densely through the exoskeleton of insect cadavers
killed by the fungus.
Beauveria bassiana has also been reported to be endophytic. It was also observed
penetration of developing hyphae on the leaf surface of Zea mays that reached the xylem
and provided insecticidal protection against damage by the European corn borer, Osirinia
nubilalis. The conidiogenous cells are usually clustered, colorless, with a globose base
and a denticulate apical extension (Humber, 2007). Conidia are 2 - 6 µm in diameter and
are borne out of zig - zag phialides or apical extensions (rachis) (Humber, 2007; Boucias
and Pendland, 2008).
5. LIFE CYCLE OF Beauveria bassiana
Beauveria bassiana is considered to be the anamorph of Cordyceps bassiana, an
ascomycete in the order Clavicipitales. The genus Cordyceps and its anamorph Beauveria
are endoparasitic pathogens of insects and other arthropods (Nikoh and Fukatsu, 2000).
Beauveria bassiana is a polymorphic fungus whose life cycle includes both single and
multicellular stages. Beauveria bassiana is an ubiquitous saprobe and can be found in soil
or decaying plant material, where it grows as multicellar mycelia by absorbing nutrients
from the decaying matter (St Germain, 2006). Reproduction and dispersion of progeny is
accomplished by the production of asexual spores called conidia. Conidia of Beauveria
bassiana are smaller than most other fungal spores measuring only 2 - 4 µm wide (Akbar
et al., 2004; Bounechada and Doumandji, 2004). Conidia are produced from conidiogenic
cells that protrude in a zig-zag structure from mycelia hyphae. Conidia released into the
environment remain dormant or in a non - vegetative state until appropriate conditions
activate germination.
Humidity is a major factor in activation of conidia independent of a host (Boucias
et al., 2008). Attachment of the conidia to the exoskeleton of a host insect also stimulates
germination. The initial attachment of Beauveria bassiana conidia to the host exoskeleton
is thought to be a function of hydrophobicity which creates a strong interaction between
the conidia surface and the waxy layer/chitonous surface of the host (Holder and
Keyhani, 2015). Germination involves the development of a hyphal structure called a
germ tube; the germ tube grows along the surface of the cuticle and can penetrate into the
cuticle by enzymatic digestion and mechanical rupture of exoskeletal components. Once
through the exoskeleton, the fungus reaches the hemolymph and there in produces single
celled morpho-types known as in vivo blastospores. These cells replicate by budding and
proliferate within the hemolymph, evading any innate immune responses (Lord et al.,
2012). When nutrients in the hemolymph are consumed the blastospores produce
elongating hyphae. These hyphae grow until they exit the cadaver and begin producing
conidia one the insect surface. The result is a fuzzy white mummified insect corpse.
6. FACTORS RESPONSIBLE FOR GERMINATION OF CONIDIA OF Beauveria
bassiana
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Germination of conidia depends largely on environmental conditions including
temperature, light and especially relative humidity. Ferron (2007) found that insects can
be infected with Beauveria bassiana at ambient relative humidities and less than 92 per
cent are required for germination and inycelial growth in vitro. He suggests that the initial
infective phase (germination on the cuticle of the insect) may be less dependent on
ambient humidity, because the microclimate of the insect cuticle is similar to that of their
host plants. The ranges of temperature and humidity for germination are broader.
Entomopathogenic fungi of Deuteromycotina infect their host via, conidia which produce
hyphae that grow directly through insect integument. In the case of Beauveria bassiana,
the most common route of infection is through the cuticle (Ferron, 2008; Pekrul and
Grula, 2009).
Temperature required for germination of Beauveria bassiana conidia ranges from
0 to 40 °C with an optimum temperature of 20 – 30 °C (Schaerffenberg, 2007; Hall,
2011; Benz, 2015). Most fungal entomopathogens require temperatures between 25 – 30
°C and relative humidity above 97 per cent for germination.
The conidia of many entomopathogenic fungi will survive in the environment
until they contact a nutritional source that will trigger germination (Smith and Grula,
2011; Ignoffo et al., 2012; Hunt et al., 2014; Gillespie and Crawford, 2015). Beauveria
bassiana germination depends on sources of carbon such as glucose, glucosamine, chitin
and starch. Nitrogen is also necessary for hyphal growth (Tanada and Kaya, 2013). Rapid
germination is desired in field situations to avoid the ill effects of ultraviolet light on the
germination and survival of the fungus (Moore and Prior, 2006; Inglis et al., 2009).
The conidia penetrate Heliothis zea (Boddie) through the spiracles and causes
infection (Pekrul and Grula, 2009). Beauveria bassiana has been reported to infect
several mosquito species through the posterior siphon and through the respiratory system
(Clark et al., 2012). Hyphae penetrate the cuticle through a series of mechanical and
enzymatic processes (Ferron, 2015). Infection of conidia through the integument depends
primarily on the nature of the cuticle, its thickness, sclerotization and the presence of
antifungal and nutritional substances (Charnley, 2009).
The entomopathogenic species of Deuteromycotina require, a relative humidity
above 90 per cent for conidial germination in vitro. Beauveria bassiana conidia
germinate in a range of temperatures between 8 °C and 35 °C, with an optimum between
25 °C and 30 °C (Tanada and Kaya, 2013).
The amount of Beauveria bassiana inoculum needs to be increased with the older
instars of larvae to achieve the same level of mortality (Fargues and Robert, 1983). Feng
et al. (2004) found first instar of Qstrinia nubilalis (Hubner) to be more susceptible to
Beauveria bassiana than later instars. It is also suggested that ingestion after penetration
of hyphae reach the homeocoel and produce hyphal bodies (blastospores) that circulate
through the hemolymph (Tanada and Kaya, 2013) and multiply by budding. Vandenberg
et al. (1998) found Diamond back moth early stages to be less susceptible to Beauveria
bassiana.
Budding continues for a period of 3 to 7 days before the fungus reverts to a
hyphal form, which infects other tissues and organs. Development of hyphal bodies in the
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hemolymph of Beauveria bassiana infected Spodotera exigua (Hubner) are known to
disrupt the cellular defense response of hemocytes (Hung and Boucias, 1992; Hung et al.,
1993). Sieglaff et al. (1997) observed less susceptibility to Metarrhizium flavoviride of
the sixth instar Schistocerca americana (Drury) than of the fourth instar.
The lack of structural components (e.g. chitin) of the hyphal bodies in the
hemolymph of Spodotera exigua larvae is an important factor for evasion of host cellular
defense mechanisms. Entomopathogenic Deuteromycotinia also produce cyclic peptides
that are found to inhibit phagocytic activity of insect plasmocytes in a dose - dependent.
Other factors influencing host susceptibility to fungal infections are the age and stage of
the insect at the time of infection, host nutrition and exposure to chemical insecticides
(Mazet et al., 1994; De Jonghe et al., 2007; Arti Prasad et al., 2010).
In order to overcome insect defenses, the fungus can also produce newer
mycotoxins. These toxins also function as antimicrobials that prevent infected silkworms
from subsequently acquiring bacterial infections. Some of these toxins are proteases that
damage the principal functions of the hemolymph or produce toxic by-products in the
insect. Other toxins are low molecular weight compounds such as beauvericin, oosporein
and bassianolide that have been demonstrated to be insecticidal (Tanada and Kaya, 2013;
Gupta et al., 1995).
Wagner and Lewis (2000) have shown that following conidia germination and
germ tube development, Beauveria bassiana enters maize tissues directly through the
plant cuticle. Subsequent hyphal growth occurs within the apoplast, but only occasionally
extending into the xylem elements. The introduction of endophytic Beauveria bassiana in
maize is compatible with other pest management strategies. It has been shown that
endophytic Beauveria bassiana is compatible with both Bacillus thuringiensis and
carbofuran applications used to suppress insect pests. Loc et al. (2002) also reported that
Metarhizium anisopliae and Beauveria bassiana used at the dose of 6 × 104 conidia/ha in
the rice fields had no adverse effect on predatory wolf spider as Lycosa peudoannulata,
Araneus inustus, Tetragnatha maxillosa, Cyrtohinus lividipennis and Polytoxus
fuscovittatus.
7. GROWTH CHARACTERISTICS OF Beauveria bassiana
Some studies made with Beauveria bassiana reveal that, the carbon sources used
for production are closely related with the spore production (Thomas et al., 1987) and
also with the spore - type produced (Hegedus et al., 1990), whereas Jackson et al. (1997)
demonstrated that, the adequate sources of carbon and nitrogen in the culture media,
would produce tolerant - desiccation blastospores of Isaria fumosorosea after air - dried
conditions; in a similar way, Sandoval Coronado et al. (2001) found that, different
supports used for formulation, such as talc, lime, gypsum or clay maintained the viability
of Isaria fumosorosea propagules to levels around 50 to 70 % for cultures obtained in
liquid media after different storage times.
7.1. Radial growth
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Kula et al. (2002) observed that the highest radial growth (4.07 cm) Metarhizium
anisopliae cultured on Sabouraud's dextrose agar with yeast (SDAY) medium for 10 days
of incubation. The growth parameters viz., radial growth, biomass and spore production
of some isolates of entomopathogenic fungi Beauveria, Verticillium and Metarrhizium
were assessed and they observed that the spore production and radial growth of
Beauveria was highest in Potato Dextrose Broth (Nirmala et al., 2005).
7.2. Spore production
Samsinakova et al. (1981), who obtained 108 conidia of Beauveria bassiana in the
medium composed of peptone 0.8 per cent and sorbitol one per cent. Rombach (1989)
recorded 7.4 × 108 blastospores ml-1 in Beauveria bassiana using the media containing
sucrose (2.5 %) and yeast extract (2.5 %).
Cherry et al. (1999) harvested dry conidial power with an average of 31.1 mg g-1
of Beauveria bassiana. Kula et al. (2002) observed highest spore count of 9.43 × 10
spores ml-1 with Metarhizium anisopliae in Earner's medium. Uma Maheswara Rao et al.
(2006) studied the impact of Beauveria bassiana on Spodoptera litura in relation to
different temperatures and pH and the initial pH of 6 - 8 to be the most suitable for spore
formation. Senthamizhselvan et al. (2010) observed that growth, sporulation and biomass
production of Beauveria bassiana was influenced by the medium used.
7.3. Growth and sporulation of Beauveria bassiana on different commodities
Basal medium containing various carbohydrate sources on growth and sporulation
of Beauveria bassiana also showed that the fungus grow best on melezitose but
sporulated best on sucrose, trehalose and D - glucose. However, least growth and
sporulation were observed on L - rhamnose and D - sorbose (Campbell et al., 1983).
Bidochka et al. (1997) reported production of blastospores of Beauveria bassiana on
liquid media containing peptone, peptone - glucose, peptone - yeast extract. Results
showed four - fold higher production of blastospores in peptone - glucose as compared to
glucose - peptone yeast extract.
Growth and sporulation of an isolate of Beauveria bassiana recorded from
Nilaparvata lugens obtained from China revealed that maximum mycelial growth of this
fungus was possible in liquid culture containing sucrose and yeast extract at 3.5 per cent
each. However, production of maximum conidia (4.62 × 106 conidia mg-1) was recorded
in the medium containing 2 per cent maltose along with 0.75 per cent yeast extract. It was
concluded that production of dry mycelia is the practical approach for mass production of
Beauveria bassiana (Rombach et al., 1988).
8. PATHOGENICITY OF Beauveria bassiana
The insect infection by fungal pathogens occurs through four successive steps.
They are contacts between the host and fungal propagules, attachment and germination of
propagules, penetration of cuticle or gut wall with subsequent invasion of host tissue and
organ and finally death of host by physical blockage of the gut, trachea, circulatory
systems, histolysis and toxin production. After the death of the host, saprophytic
development of fungus is necessary for the completion of pathogenic cycle. A fungus,
unlike other microbials does not require ingestion for infection in the host - Infection
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through mouth parts, and orifice, digestive and genital tracts have also been reported
(Ferron, 2008).
The fungal pathogenesis begins with adhesion of conidia to the cuticle of host
followed by germination of conidia which penetrates the cuticle through germ tube. The
germ tube passes through the integument of insect. Finally, the fungus develops inside
the body of host which results in death of the host insect. Under suitable environmental
conditions, death was followed by external sporulation of fungus (Moore and Prior,
2006). The infection of insects by entomopathogenic fungi occurs following germination
of conidia/spores on the cuticle and it penetrates through the integument (Clarkson et al.,
1998).
Clark et al. (2012) reported that the formation of germ tube on the integument of
host, penetration of cuticle by penetration peg is usually followed by formation of
appresorium that finally attach the fungus to the epicuticle and provides basic support for
mechanical and enzymatic process through epicuticle, penetrant hyphae and penetrant
plates develop in the procuticle which produce hyphae that give rise to both irregular and
smooth walled hyphal bodies. The two primary infection sites were the head and the anal
region and the most preferred site for fungal development was the larval gut (Miranpuri
and Khachatourians, 2007).
The hyphal bodies of Beauveria bassiana produce hyphae, which ultimately
penetrate the procuticle and move to haemocoel (Hajek et al., 2001). The hyphal bodies
which are single or multinucleated structures without cell wall but contain a thin fibrillar
layer with plasma membrane (Referred as blastospores) that produce new hyphae that
ultimately fill the body cavity and remain as resting spores in the dead host.
Ferron et al. (1991) observed that selection of fungal pathogens tolerant to the
temperature range in the ecosystem in which they are to be used is imperative for their
use as mycopesticides. Doberski (1981) selected fungal strains with pathogenic activity
below 15 °C for insect pests in temperate regions; McClatchie et al. (1994) chose strains
active at temperatures >30 °C for use against desert locusts in West Africa. Similarly,
Mohammed et al. (1977) sought isolates adapted to temperatures >25 °C for control of
noctuid insects in the southeastern USA.
9. Beauveria bassiana AS A BIOCONTROL AGENT
As agricultural pests present an economic and resource production problem to
human society, other arthropod pests are a direct human health concern. In this regards, a
number of parasitic arthropods act as vectors for the transmission of infectious diseases.
Because of their ability to access the human circulatory system, blood feeding arthropods,
are important vectors by which microbial parasites can be transmitted between various
hosts. Beauveria bassiana shows potential for controlling arthropod disease vectors, and
hence has the potential to decrease the spread of diseases carried by these insects. Ticks
are an example of an arthropod that can carry and transmit a wide variety of disease
causing agents. Ticks, obligate blood feeders, are potential carriers of the bacteria
Borrelia burgdorferi, the causative agent of Lyme disease in humans and domestic
animals (Stricker et al., 2006). Other tick born diseases include; Rickettsia rickettsii,
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causative agent of Rocky Mountains spotted fever in both humans and some domestic
animals; Babesia canis and Babesia gibsoni, a protozoan parasite of domestic animals;
and several species of the genus Ehrlichia, an obligate intracellular cocci responsible for
a variety of blood cell diseases in domestic animals (Ettinger, 2000; Waner, 2001).
Research studies have shown that the prominent tick species including those known to
transmit Lyme disease are susceptible to infection by Beauveria bassiana (Kirkland et
al., 2014).
Chagas disease is a parasite infection that is transmitted by an insect vector,
primarily the South American kissing bug (Triatoma infestans) (Lazzarini et al., 2006).
Chagas disease is a serious health problem in South America where approximately 20
million people are infected. The health costs associated with treating an infection is often
too high for the majority of those inflicted with the disease. For this reason, research into
the control and prevention of the disease is focused on vector control and involving the
use of Beauveria bassiana and other entomopathogenic fungi. Brazil and Argentina are
two countries with research facilities studying the pathogenicity of Beauveria toward
these insect disease vectors (Luz and Fargues, 1998; Luz et al., 1998; Marti et al., 2005).
Beauveria bassiana occurs worldwide and it is the most frequent species isolated
from insects and soil samples, where it can survive for long periods in saprogenesis.
Under laboratory conditions, it can colonize the majority of insects, occurring
enzootically and epizootically in the field. The infection occurs naturally via tegument,
where the fungi germinate within 12 to 18 hrs, depending on the presence of nutrients,
such as glucose, chitin, and nitrogen among others (Alves, 1998).
Beauveria bassiana may also be a valuable tool in the fight against malaria.
Between 300 and 500 million people are infected with malaria, and this disease is
responsible for as many 1.5 million deaths annually (Geetha and Balaraman, 1999;
O'Hollaren, 2006). Currently, there are no vaccines against malaria; however, studies
have shown the potential for fungal entomopathogens to reduce the spread of this disease
(Blanford et al., 2005; Scholte et al., 2005). In this regard, the use of entomopathogenic
fungi resulting in the infection of as little as 23 % of the indoor mosquitoes reduced the
yearly number of bites received by residents by as much as 75 %. Indoor treatment
combined with outdoor applications to control mosquito populations at “hot spots” it is
projected that bites by mosquitoes could be lowered by as much as 96 % (Scholte et al.,
2004; Scholte et al., 2005).
Bittencourt et al. (1997) have evaluated the action of different isolates of
Beauveria bassiana and Metarhizium anisopliae fungi on distinct stages of Beauveria
microplus, proving their in vitro pathogenicity to this tick species. The entomopathogenic
action of Beauveria bassiana has also been demonstrated for other tick species such as
Rhipicephalus sanguineus (Monteiro, 1997), Amblyomma cajennense and Boophilus
decoloratus (Kaaya and Hassan, 2000). According to Kaaya and Hassan (2000), the use
of entomopathogenic fungi to control ticks may reduce the frequency of chemical
acaricide use and the need for treatment for tick-borne diseases. These authors also
conclude that mycopesticides are safer for the environment than conventional acaricides.
10. SOLID AND DIPHASIC PRODUCTION TECHNOLOGIES
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The genus Beauveria is a parasite of a great number of arthropods, occurring in
more than 200 species of insects and acaridae. These entomopathogenic fungi may occur
in enzootic and epizootic forms in field or produced in vitro through fermentative
processes (Alves, 1998). Solid State fermentation (SSF) may be defined as the growth of
microorganisms in solid substrates in the absence of free water. The free water is found in
the complexes form in the interior of a solid matrix (Lonsane et al., 1985; Pandey et al.,
2001; Soccol and Vandenberghe, 2003).
Solid State fermentation may be classified by the function of the solid phase; it
can serve only as a support for the growth of microorganisms and be inert for nutritional
purposes and in such case the nutritive sources necessary for the growth of
microorganisms are adsorbed by the support. The solid phase may be the support and at
the same time the substrate for fermentation. In this case, the support gives also the
nutrients required for the growth of microorganisms (Brand et al., 2000). Solid State
fermentation shows advantages for the production of spores in short period of time, due
to its simplicity in comparison with submerged cultivation. To make the production of
fungal spores process at semi-industrial scale viable, it is necessary to obtain an ideal,
cheap and highly productive culture media, which maintain morphological,
pathogenically and virulogically characteristics.
These are several studies on the efficient utilization of agro-industrial residues
with value addition (Soccol and Vandenberghe, 2003; Soccol, 1994; Pandey et al., 2001).
The residues could be utilized as substrates and support for the production of citric acid
(Vandenberghe et al., 1999); biological detoxification of coffee husk for the production
of animal feed (Brand et al., 2000), edible mushrooms (Leifa et al., 2000), enzymes and
ethanol; reducing in this way environmental pollution problem that the disposal of this
residues may cause (Pandey et al., 2001).
Diverse raw materials have been tested for the production of entomopathogenic
fungi, such as caupi, sorgo, broad bean, beans, cassava bagasse, rye flour, cassava flour,
different types of rice and residues such as sugar - cane bagasse enriched with cane syrup
and torula residues, or still refused potatoes are utilized (Burtet et al., 1997; Soccol et al.,
2003; Vilas Boas et al., 1996; Calderon et al., 1995). With high carbohydrates, proteins
and significant amounts of salts and vitamins, potato has a high nutritional value
(Trindade, 1994).
Production of adequate quantities of a good quality inoculum is an essential
component of the biocontrol programme. The production of entomopathogens may be
taken up by the following methods based on the quantity of the product desired: 1)
relatively small quantities of the inoculum for laboratory experimentation and field –
testing during the development of mycopesticide and 2) development of a basic
production system for large - scale production by following the labour intensive and
economically viable methods for relatively small size markets. China (Feng et al., 2004)
and America (Alves and Pereira, 1989) are supplier of fungal pathogens by this method
in sufficient quantities for niche markets in their immediate area.
Development of simple and reliable production system follows the basic
multiplication procedures of submerged liquid fermentation for the production of
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blastospores, which are short lived and hydrophilic (Rombach, 1989) or solid state
fermentation (Rousson et al., 1983) for the production of aerial conidia. However, the
most viable mass production technologies include making use of a diphasic strategy in
which the fungal inoculum is produced in liquid culture, which is further utilized for
inoculating the solid substrates for conidia production (Burges and Hussey, 1981).
The insect infection by fungal pathogens occurs through four successive steps.
They are contacts between the host and fungal propagules, attachment and germination of
propagules, penetration of cuticle or gut wall with subsequent invasion of host tissue and
organ and finally death of host by physical blockage of the gut, trachea, circulatory
systems, histolysis and toxin production. After the death of the host, saprophytic
development of fungus is necessary for the completion of pathogenic cycle. A fungus,
unlike other microbials does not require ingestion for infection in the host- Infection
through mouth parts, and orifice, digestive and genital tracts have also been reported
(Ferron, 2008).
The fungal pathogenesis begins with adhesion of conidia to the cuticle of host
followed by germination of conidia which penetrates the cuticle through germ tube. The
germ tube passes through the integument of insect. Finally the fungus develops inside the
body of host which results in death of the host insect. Under suitable environmental
conditions, death is followed by external sporulation of fungus (Moore and Prior, 2006).
According to Moore et al. (2000), fungal spores are living organisms and their
viability diminishes with time depending on environmental conditions. It is therefore
essential to determine the best substrate for spore production and their viability. Previous
studies by Kutywayo et al. (2005) revealed that the three isolates were unique and had
potential as biocontrol agents. The author also determined the suitable temperature for
spore production as 28 °C.
11. BLASTOSPORE PRODUCTION OF Beauveria bassiana
Blastospores are produced during the fermentation process in commercial
production of spores where as aerial spores are produced on conidiogenous cells on the
infected insects. However the pathogenicity of blastospores and aerial spores is same.
The death of insect may result due to non - availability of nutrients, invasion of organs by
fungus and toxicosis due to toxins produced by Beauveria bassiana. After the death of
the insect, fungus grows saprophytically inside the body of the insects and produces
metabolites that may not allow other competing microbes to grow in the cadaver. It
reproduces sexually in soils throughout the world and asexually in a variety of insect
hosts. In its asexual form it produces spores known as conidia which are wind dispersed.
Once they are released they may land upon another insect host, or once again return to
the soil where they reproduce sexually retaining the properties which make it an effective
pest control, and preventing the qualities which cause it to be harmful to beneficial
insects (Boucias and Pendland, 2008).
Blastospore production using liquid culture fermentation is vegetative fungal
propagules that are the preferred mode of growth for many entomopathogens in the
haemocoel of infected insects (Shimuzu et al., 1993; Sieglaff et al., 1997; Vestergaard et
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al., 1999; Askary et al., 1999). Yeast - like growth allows the fungus better access to the
nutrients within the insect. Numerous entomopathogens of the genera Beanveria can be
induced to grow in a 'yeast - like' fashion in submerged liquid culture. Blastospore based
mycoinsecticides are currently produced commercially by Beauveria bassiana.
The impact of nutrition on conidial yields for various fungal entomopathogens in
liquid culture was found to be significant (Vega et al., 2003). Poly Ethylene Glycol
incorporation in the media increased the blastospores and curtailed the mycelial pellet
development (Sreeramakumar et al., 2005).
The optimization of glycerol and erithritol in the conidia increases germination
and increase spore longevity of blastospore, in addition to conferring greater osmotic
tolerance. The deuteromycete Beauveria bassiana should be included in the list of
versatile deuteromycetes that store carbohydrates, including glycogen and the polyols
mannitol, erythritol, glycerol and arabitol (Bidochka et al., 1990; Hallsworth and Magan,
1995; Faria and Wraight, 2007).
Glycerol, erythritol, arabitol and manniiol accumulate in fungal cells at low level.
Intracellular accumulation of these polyols reduces cytoplasrnic activity and yet does not
disrupt enzyme structure and function, thus allowing metabolic activity to continue
during periods of low water availability (Brown, 1978; Beever and Laracy, 1986; Van
Eck et al., 1993).
Humphreys et al. (1989) grew this entomopatbogenic fungus in submerged liquid
culture on glucose and polyethylene glycol - adjusted media of differential water
activities. They recorded increase in yield of blastospores of fed batch liquid culture of
Beauveria bassiana when water activity of the nutrient feed was reduced by the addition
of 2.4 MPEG. According to Vega et al. (2009), the highest spore yields of Beauveria
bassiana in liquid concentration of 36 g L-1 and a C: N ratio of 10: 1 using sucrose and
casamino acid.
CSL contains water (46 %), proteins (47 %), amino acids, minerals, vitamins,
reducing sugars, organic acids, enzymes, fat and elemental nutrients (White and Johnson,
2003). These constituents can be readily assimilated into normal cell metabolism. The
blastospore production of Metarhizium flavoviride Mfl89 was based on sucrose and
brewer's yeast, with a C: N ratio of 1: 6 (Issaly et al., 2005).
12. FORMULATIONS OF Beauveria bassiana
The development of a suitable formulation is essential to the successful utilization
of commercial mycoinsecticides (Daoust et al., 1983). For example, many formulations
can affect the conidial viability resulting in a short shelf life (Moore and Prior, 1993).
There is a need for careful assessment of the compatibility of formulation components
with conidia prior to their use in formulations (Daoust et al., 1983). Therefore, one of the
first steps in developing a mycoinsecticide formulation is to evaluate the effects of its
components on conidial viability to select products compatible with fungal conidia. The
development of fungal pathogen formulation depends on fungal strains, mass production
ability and appropriate climate region (Butt et al., 2001). The most important factors
limiting the use of fungi as an insecticide were solar ultraviolet radiation, temperature,
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humidity and their ability on spreading on the surface (Stathers et al., 1993). Formulating
pathogens in oil enhances their infectivity compared to conventional water - based
formulations (Agudelo and Falcon, 1983; Prior et al., 1988; Bateman et al., 1993).
Knudsen et al. (1990) formulated the Beauveria bassiana mycelium in granules of
sodium alginate with and without the addition of ground wheat. After five months of
storage at room temperature, the fungi with most spore production came from the
granules with wheat, with 2.45 × 108 conidia per granule. These, once placed on
seedlings of wheat infested with Schizaphis graminum Rondani, caused the death of three
to forty-four percent of aphis, against zero percent in the control.
In general, temperature and moisture content, or the humidity of the storage
atmosphere is the major factors which influence conidial longevity (Hong et al., 1997).
Hedgecock et al. (1995) studied the influence of moisture content on temperature
tolerance and storage of Metarhizium anisopliae var. acridum in oil formulation and the
results demonstrated that viability declined due to high temperatures and high moisture
contents. Drying the conidia with silica gel greatly improved high temperature tolerance
(McClatchie et al., 1994). The optimal moisture content for dried conidia storage was
found to be 4 to 5 % and a range of mineral oils proved satisfactory for dried conidia
storage (Moore et al., 1996). Less moisture content than 4 to 5% may give better results
but it is difficult to achieve.
Suspo-emulsions can be defined as heterogeneous formulations consisting of a
stable dispersion of active ingredients in the form of solid particles and of fine globules in
a continuous water phase combinations (GCPF, 1994). They are relatively new to the
agricultural market and have a great potential for formulation and application of
mycoinsecticides for pest control. They can be sprayed by very low volume/controlled
droplet application techniques still allow the use of conventional hydraulic sprayers and
nozzles and water - the cheapest and most readily available carrier liquid for pesticides
(Alves et al., 1998).
In the field, efficiency of entomopathogens depends up on virulency towards
target insect, coverage and persistence on target site. However, major constraints for
successful use of such bioagents are their short shelf - life and dependability on the
prevailing environmental conditions (Kaur et al., 1999). The foregoing problem can
largely be overcome by developing suitable formulation technology. The performance
and shelf - life can be improved by adding suitable ingredients that may act as nutrient,
adhesive or wettable agents. Xutrilite products Inc., Buena parts. California., U.S.A were
the first company in U.S.A to develop both dust and wettable powder formulations of
Beauveria bassiana for research purpose (Dunn and Mechalas, 1963).
Scientists of USSR also developed dust formulation of this fungus as boverin
using inert materials like talc or perlite, kaolin, bentonite, starch etc., (Ignoffo et al.,
2009). Pereira and Roberts (1991) reported that corn starch with oil formulation produced
more conidia from each gram of incorporated mycelia while alginate formulation could
protect the fungus better from artificial solar radiation as compared to corn starch oil.
The liquid formulations were prepared by supplementing polymers which
increased the spore longevity, viability thereby the shelf - life of the organism is
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increased. The studies on liquid formulation are detailed hereunder. Addition of certain
polymers in growth media is one of the various techniques through which mycelia pellet
formation can be decreased by encouraging diffuse mycelia growth or formation of tiny
hyphal fragments or blastospores for liquid formulation (Bidochka et al., 1990).
Kleepspies and Zimmermann (1992) have also obtained increased blastospore production
and reduced pellet formation of Metarhizium anisopliae (Metschn.) Sorokin using PEG
200. Tween 80 and high or low pH. Inch and Trinci (1987) and Humphreys et al. (1989)
reported that the addition of PEG 200 suppressed the formation of pellets in liquid
cultures of certain entomopathogenic fungi having commercial value.
Knudsen et al. (1991) reported that conidia production of Beauveria bassiana
was very fast in alginate pellets with polyethylene glycol 8000 coated wheat bran as
compared to uncoated pellets. Geetha and Balaraman (2001) reported that PEG (2 %)
favoured both higher biomass and blastospores in the case of Beauveria bassiana. Poly
Ethylene Glycol at 6 per cent concentration in Sabouraud's Dextrose Agar influenced
both quality and quantity of the biomass of Hirsutella thompsonii (non - synnematous)
and Hirsutella thompsonii var. Synnematosa (synnematous) fungi in submerged culture
(Sreeramakumar et al., 2005).
Efficacy of Beauveria bassiana combined with various stickers or spreaders
revealed very high percentage of mortality of Dicladispa armigera using Tween-80
(Puzari and Hazarika, 1991). Use of two formulations of mineral oil (Emulsiflable
concentrate and emulsion concentrate) containing Beauveria bassiana in the laboratory at
26 °C and 70 per cent relative humidity resulted in 77.5 and 100 per cent mortality,
respectively as compared to 38 per cent caused by fungus alone at 16 days after treatment
(Batista et al., 1994).
Inglis et al. (1996) investigated the efficacy of two formulations (oil and water)
and two bait substrates (Lettuce and bran containing Beauveria bassiana) against the
nymphs of Metarhizium sanguinipes. Based on their experiment they reported superiority
of oil formulations over water formulations; while no differences in mortality was
observed between lettuce and bran substrates. Formulation of conidia of the Beauveria
bassiana in paraffin oil or dried powder showed greater percentage of germination of the
sample stored in dry conditions as compared to oil formulation of different temperature
viz., 10 °C, 20 °C, 30 °C, 40 °C and 50 °C.
Smith et al. (1999) also tested aggregation phremone in the vegetable fat pellets
(hydrogenated rapeseed oil) containing Beauveria bassiana as formulation against
Prostephenus truncates under laboratory. The investigation on stability of the
formulation sodium alginate and pregelatinized corn starch at different temperatures for
120 days revealed the suitability of pregelatinized corn starch for the formulation with
mycelia of Beauveria bassiana (Marques et al., 1999). The use of formulations
containing Beauveria bassiana is an eco-friendly approach, especially due to proper
understanding of problems due to indiscriminate use of insecticides in many countries in
the last environmental hazards, insect resistance to insecticides, sustainability in crop
productive, pesticide free organic food and maintenance of biodiversity.
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13. AGRICULTURAL IMPORTANCE OF Beauveria bassiana
Agricultural pests continue to be a major problem, responsible for tremendous
losses in productivity. Traditionally, chemical pesticides such as DDT (dichlorodiphenyl
- trichloroethane) and endosulfan have been used to kill unwanted insects. The use of
chemical pesticides, however, has resulted in numerous problems. Many insects develop
resistance to chemical poisons making these compounds less effective and therefore
required in higher concentrations. Furthermore, extensive application of chemicals into
the environment often has deleterious effects on non - target organisms including
beneficial insects such as pollinators and natural predators of the target pest. Finally,
chemical pesticides display significant health risks to workers who are exposed to the
chemicals in the fields as well as to consumers who purchase food products with residual
pesticides. Thus, there is great interest in alternatives to chemical pesticides.
The use of biological pesticides such as entomopathogenic fungi is growing in
popularity because it is able to alleviate many of the concerns associated with chemical
poisons. First, entomopathogenic fungi are found ubiquitously in the soil throughout the
world, therefore they would not be considered as “introduced” organisms into the
environment. Second, although Beauveria bassiana is considered a broad - spectrum
insect pathogen, strains can be developed that are more hosts specific. With research into
pathogenicity and strain specificity, it is anticipated that fungal biological control agents
can be selected to target specific insect pest.
Entomopathogenic fungi are effective and environmentally safe biological control
agents that can be used against many important pest species in both agriculture and
forestry because they are safe for animals, plants and environment (Chandler et al., 2000;
Shah and Pell, 2003; Gokce and Er, 2005; Goettel et al., 2015). Entomopathogenic fungi
differ from other insect pathogens since they are able to infect through the host’s
integument, therefore ingestion is unnecessary and infection is not limited to chewing
insects. Therefore, they are unique to control insect pests which feed by sucking plant or
animal fluid (St Leger and Roberts, 1997).
Entomopathogenic fungal species belong to Beauveria genus attack many insect
pests worldwide and species within the genus range from the ubiquitous insect pathogen
such as Beauveria bassiana to rare species. However, the entomopathogenic life - style is
dominant (Glare et al., 2008; Sevim et al., 2010; Glare, 2014). A total of six species were
described within this genus and they were designated as Beauveria bassiana, Beauveria
bassiana cf. Clade C, Beauveria brongniartii, Beauveria caledonica, Beauveria
vermiconia and Beauveria amorpha (Glare and Inwood, 2004; Glare and Inwood, 2008;
Sevim et al., 2010; Glare, 2014; Rehner and Buckley, 2015). Among these species,
Beauveria bassiana is the most studied one and remarkable effort were spent to develop
microbial control agent using this species. Moreover, the most widely used species
available commercially is Beauveria bassiana (Meyling and Eilenberg, 2007; Goettel et
al., 2015). The entomopathogenic fungus Beauveria bassiana is extensively used for the
control of many important pests of various crops around the world and it was tested on
different target insects (Campbell et al., 1985; Leathers and Gupta, 1993; Padmaja and
Kaur, 2001; Todorova et al., 2002; Tafoya et al., 2004; Sevim et al., 2010).
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There are extensive efforts to develop Beauveria as a biological agent. Beauveria
has been examined as a potential biological control agent of Ocneridia volxemi. A species
of grasshopper, Ocneridia volxemi is one of the most destructive pests of cereals crops in
Algeria (Bounechada and Doumandji, 2004). Beauveria is also being examined as
method to control the citrus rust mite, Phyllocoptruta oleivora, a citrus crop pest of South
America (Alves et al., 2005). One of the most destructive pests being targeted by
application of Beauveria control is the coffee berry borer (Hypothenemus hampei), which
is endemic to most coffee growing regions and results in upto 40 % losses of the crop.
Hypothenemus hampei is an agricultural pest responsible for hundreds of millions
of dollars in losses by coffee growers each year (Posada et al., 2004). Beauveria was
studied around the world as an effective control agent of coffee berry borer including
research facilities found in Honduras, Brazil, Mexico and India (Fernandez, 1985;
Haraprasad, 2001). Due to the illegalization of some pesticides including enosulfan;
Columbia is an example of a country that utilizes Beauveria against this pest (Cruz et al.,
2005).
Beauveria bassiana as well as Metarhizium anisopliae are under investigation and
show promise for the control of the tobacco spider mite. The tobacco spider mite is one
of several species of mites belonging to the genus Tetranychus. Found throughout the
United States Tetranychus mites are responsible for the destruction of crops ranging from
fruits and vegetables to cotton and decorative plants. Studies showed that the treatment of
mite-infected tomato plants with conidia of these entomopathogens greatly reduced the
number of mites on the treated plants as compared to untreated plants (Wekesa et al.,
2005).
Dirlbek et al. (1989) observed slightly better results when Boverol (Beauveria
bassiana) used @ 0.3 per cent in combination with delta methrin 2.5 EC @ 0.016 per
cent against Trialeurodes vaporarionim while good reduction in pest population resulted
when methidathion 40 wp was added.
The fungus Beauveria bassiana was effective against Ostrinia nubilalis and the
damage caused by the larvae to plant and ears reduced by 50 per cent as compared to the
control (Yashugina, 1970). Soil application of Beauveria bassiana and Paecilomyces
farinosus, resulted in significant reduction in population of Leptinotarsa decemlineata
(Bajan et al., 1973). Beauveria bassiana @ 1.32 to 1.8 kg ha-1 mixed with sevin
(Carbaryl) @ 0.14 kg ha-1 or chlorofos @ 0.078 kg ha-1 provided 58.1 to 75.5 and 73.3 to
86.3 per cent: control Carpocapsa pomonella and Hoplocampa testudinea, respectively
(Prieditis and Rituma, 1974).
Use of parasitoid Trichogramma sp., the microbial pathogen Bacillus
thuringiensis and Beauveria bassiana along with insecticides trichlorophon (Chlorofos)
against Mamestra brassicae, Pieris brassicae and Plutella xylostella resulted in increase
in yield of cabbage by 6 to 7 per cent. Three application of low doses of both Boverin
(Beauveria bassiana) and trichlorophon (Chlorofos) on egg plants produced excellent
control of Leptinotarsa decemlineata throughout the season, which resulted in substantial
increase in yield.
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The Beauveria. bassiana was effective against Nilapawata lugens @ 4 × 10 to 5
× 10 conidia ml-1. The fungus produced 63 - 98 per cent mortality 3 weeks after
application (Rombach, 1989). The dry mycelium of Beauveria bassiana @ 200 and 2000
g ha-1 and the conidia @ 7.5 × 10 ha-1 had significant control over Nilaparvata lugens
(Aguda et al., 1987; Pham et al., 1994).
Purwar and Sachan (2005) studied the impact of different isolate such as
Pantnagar isolates and IMTECH strains of Beauveria bassiana and Metarhizium
anisopliae on Spilarctia iitura and Spilarctia obliqua. Uma Maheswara Rao et al. (2006)
also studied the impact of Beauveria bassiana on Spilarctia litura in relation to different
temperatures.
14. CONCLUSION
From the present review, it was concluded that the various formulation of
entomopathogenic fungi Beauveria bassiana was highly effective against various insect
pests which causes heavy economic loss to the agricultural crops when compared to the
commercial synthetic insecticides. The entomopathogenic fungi Beauveria bassiana also
reduces the larval population and crop damage caused by target pests and increases the
yield of agricultural crops particularly vegetable crops. Application of entomopathogenic
fungi Beauveria bassiana in agricultural fields for the control of insect larvae and pests
was cost – effective, increases the yield of agricultural products, minimizes the usage of
chemical pesticides and prevent the environment from the pesticide pollution.
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