ISSN: 2454-1370

Available online at www.jpsscientificpublications.com

Volume – 3; Issue - 2; Year – 2017; Page: 1051 – 1087

DOI: 10.22192/iajmr.2017.3.2.4

Indo – Asian Journal of Multidisciplinary Research (IAJMR)

ISSN: 2454-1370

© 2017 Published by JPS Scientific Publications Ltd. All Rights Reserved

AGROBENEFICIAL ENTOMOPATHOGENIC FUNGI – Beauveria bassiana:

A REVIEW

P. Saranraj*1 and A. Jayaprakash

2,

1Assistant Professor of Microbiology, Department of Biochemistry, Sacred Heart College (Autonomous),

Tirupattur – 635 601, Tamil Nadu, India. 2Department of Biochemistry, Sacred Heart College (Autonomous), Tirupattur – 635 601, 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.

________________________________________________________________________________

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

*Corresponding author: Dr. P. Saranraj Received: 20.01.2017; Revised: 22.02.2017; Accepted: 13.03.2017.

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.

http://www.jpsscientificpublications.com/

P. Saranraj/Indo – Asian Journal of Multidisciplinary Research (IAJMR), 3(2): 1051 – 1087 1052


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 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

agroecosystem (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).

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 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 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 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 cyclo-

octadepsipeptide, 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 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 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 bassiana 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 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 and 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 - 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

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

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. 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, 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.

Radial growth

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).

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 (1988) 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.

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

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, 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).

Chaga’s disease is a parasite infection

that is transmitted by an insect vector, primarily

the South American kissing bug (Triatoma

infestans) (Lazzarini et al., 2006). Chaga’s

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 & Diphasic production technologies

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,

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) is 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 blastospores,

which are short lived and hydrophilic (Romback,

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 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 (Sree

Ramakumar 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 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 (Beever and

Laracy, 1986; Van Eck et al., 1993). Humphreys

et al. (1989) grew the entomopathogenic 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 was 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 was 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, 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 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).

Inglish 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.

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 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. 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; Goettel et al., 2015; Gokce and Er,

2005). 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, 2014; Glare et al., 2008; Sevim et al.,

2010). 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, 2008;

Glare and Inwood, 2004; Glare, 2014; Rehner

and Buckley, 2015; Sevim et al., 2010). 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).

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 (Garnaga, 1975).

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.

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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DOI: 10.22192/iajmr.2017.3.2.4

How to Cite this Article:

P. Saranraj and A. Jayaprakash. 2017.

Agrobeneficial Entomopathogenic Fungi –

Beauveria bassiana: A Review. Indo - Asian

Journal of Multidisciplinary Research, 3 (2):

1051 – 1087.

DOI: 10.22192/iajmr.2017.3.2.4

http://www.jpsscientificpublications.com/

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