journal of entomology

OPEN ACCESS Journal of Entomology

ISSN 1812-5670DOI: 10.3923/je.2020.74.83

Review ArticleEntomopathogenic Fungi: Factors Involved in Successful MicrobialControl of Insect Pests1Ghulam Ali Bugti, 3Wang Bin, 1Shafique Ahmed Memon, 2Ghulam Khaliq and 2Muhammad Abuzar Jaffar

1Department of Entomology, Lasbela University of Agriculture, Water and Marine Sciences, Uthal, Balochistan, Pakistan2Department of Horticulture, Lasbela University of Agriculture, Water and Marine Sciences, Uthal, Balochistan, Pakistan3Anhui Provincial Key Laboratory of Microbial Control, Anhui Agricultural University, People Republic of China

AbstractEntomopathogenic fungi have great potential to control insect pests, which either feed on aerial or underground plant parts. The studyrevealed that virulence and pathogenicity of fungi greatly affected by biotic factors such as fungal species, spore density, host plantchemistry, insect host species and host life stages and abiotic factors likewise, temperature, sunlight, rain and relative humidity. The aimof this review is to find out the factors and characteristics which affect the virulence and pathogenicity of the fungi. From the literature,it was concluded that the relative humidity seems to be more important than other factors to ensure infection and successful diseasedevelopment in targeted insect population.

Key words: Entomopathogenic fungi, biotic abiotic factors, Pathogenicity, insect pests

Citation: Ghulam Ali Bugti, Wang Bin, Shafique Ahmed Memon, Ghulam Khaliq and Muhammad Abuzar Jaffar, 2020. Entomopathogenic fungi: factorsinvolved in successful microbial control of insect pests. J. Entomol., 17: 74-83.

Corresponding Author: Ghulam Ali Bugti, Department of Entomology, Lasbela University of Agriculture, Water and Marine Sciences, Uthal, Balochistan,Pakistan

Copyright: © 2020 Ghulam Ali Bugti et al. This is an open access article distributed under the terms of the creative commons attribution License, whichpermits unrestricted use, distribution and reproduction in any medium, provided the original author and source are credited.

Competing Interest: The authors have declared that no competing interest exists.

Data Availability: All relevant data are within the paper and its supporting information files.

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J. Entomol., 17 (2): 74-83, 2020

INTRODUCTION

Approximately one thousand insect pathogenic fungalspecies have been known to infect various insects species1.About 100 conidia based insecticides are registered worldwideto control many serious insect pests of agriculture2. Thesefungi can produce different enzymes and secondarymetabolites which help insect infection development and alsoplay and vital insecticidal role3. As insect cuticle contains up to70% of protein, the penetration development is facilitated byfungal proteases like; trypsins, chymotrypsins,metalloproteases and subtilisins, these toxic metabolites withinsecticidal effect include substances released by differententomopathogenic fungi such as; detrains produced byMetarhizium species, beauvericins, isarolides, bassianolides,beauverolides oosporein produced by Beauveria species orIsaria fumosorosea, efrapeptins produced by Tolypocladiumspecies and hirsutellin released from Hirsutella thompsonii4-6.The existence of entomopathogenic fungi is quite wide andcan be found almost all over the world (e.g., tropical rainforest,Antarctica or Arctic), so they are a worldwide spread group offungi7,8.In temperate regions of the world, the order hypocreales

and entomophthorales are generally known infectious tomany insect species. The hypocrealean species B. bassianaand M. anisopliae are known to infect many insect speciesrelated to agro-ecosystems9,10. Recent advance studies onentomopathogenic fungi clarified the importance of fungi asa conservation microbial control agent against many insectpests of field crops and forest trees. It is reported that most ofB. bassiana species associated with insect pests above groundlevel, while M. anisopliaeis associated either on orunderground11-13.Entomopathogenic fungi occur in nature and are capable

to cause epizootics and decrease the insect population andrepresent a larger portion of present bio-pesticide in themarket worldwide14-17. Viewing importance ofentomopathogenic fungi in insect control the current reviewarticle is compiled to find out the hurdles/factors which effecton the virulence and pathogenicity of entomopathogenicfungi. This review will provide useful information regardingentomopathogenic fungi and their success in variousenvironmental conditions.

CHARACTERISTICS AFFECTINGVIRULENCE OF FUNGI

Fungal taxonomy: Literature indicated that insect-pathogenicfungi are true fungi and belongs to different phylum i.e.,Ascomycota, Zygomycota, Chytridiomycota and

Basidiomycota Coelomomyces, among these the genusChytridiomycota known as a good aquatic entomopathogenicspecies which produce zoospores asexually and significantlyaffect the many Dipterian insects including mosquitoes. TheZygomycota phylum is further divided into sub-divisionsZygomycotina, class Zygomycetes and orderEntomophthorales18,1. These fungi are capable to infect variousinsect species. In case of unavailability of suitable host, mostof fungi have ability to produce motionless spores, which alsocan live under unfavourable conditions. For example, duringwinter season these spores either produced sexually orasexually. The well-known common genera are Neozygites,Erynia, Zoophthora, Conidiobolus and Entomophaga19,20.While a larger portion of Entomophthorales are host-specific,e.g., Entomophthorales Neoaphidis species only reportedfrom aphids. Whereas, Zoophthora radicans (Brefeld) Batkowas documented from different insect species, however, mostof the individual isolate infect particular insect species21. TheDeuteromycotina is the main group of entomopathogen andknown as “Imperfecti”. The reproduction in classHyphomycetes took place asexually, however, sexualproduction is occurred rarely. The sexual behaviour occurs insome species of Cordyceps, but some researchers suggestedthat these species should be placed in the group ofAscomycota22. The fungus Deuteromycotina does not produceinactive spores and has the ability to survive in the soil23.The well-known Entomopathogeneous fungi which

belong to class Hyphomycetes are Verticillium, Metarhizium,Aschersonia, Beauveria, Paecilomyces, Nomuraea andHirsutella. Among these the most popular species is Beauveriathat cause “white muscardine” disease9,24,25. As being a goodpathogenic fungus the many studies were conducted in thisgenus that is V. lecanii26, whereas, the genus Metarhiziumknown as “green muscardine” fungus, reviewed anddocumented by Kryukov et al.27. Entomopathogenic fungi arefungi having denticulate (tooth-like or bristle-like structure)apical extensions (rachis) containing single conidium perdenticle and conidia are a-septate. Conidia of B. bassiana areapproximately round ball-shaped about <3.5 pm diameter,whereas, Isaria fumosorosea conidia are grown individually orin clusters form on ringlets on branches of conidiophoresor on short side branches or in apical whorls conidia area-septate and range from colorless pigment. Conidia of Isariafumosorosea are long, ovoid and <4 pm long28.

For example, Isaria farinos a need carbon and nitrogen forstimulating growth and developmental stage of germ tube29.The germ tube penetrates into insect body through hyphae30.The developmental stage of an “appressorium” thickenedflattened most upper tip of a hyphal out-growth, which assistthe fungi to bind and penetrate into host cuticle31. Some of

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J. Entomol., 17 (2): 74-83, 2020

Density and spatial distribution of spore in relation to release or

inoculation strategy

Host life stage

Economic injury level

Susceptibility

Host characteristics Fungal characteristics

Host rang

Virulence

Sporulation

Persistence

Epizooticpotential

Compatibility with otherpest and disease control

Toxicological and safety aspects

Suitability forstorage andformulation

DispersalPossibilities formass production

Fig. 1: Host and fungal characteristic effect on pathogenicity and infection process of fungi

hyphomycetes fungi can cause death before the extensiveintrusion of insect tissues. These types of entomopathogenicfungi cause mortality by releasing toxic substances12,32. Afterinfection, the fungal spore emerges from insect cuticle andstarts sporulation on the insect dead body. Many fungalhyphae primarily grow inside the inter-segmental regions ofthe host. This provides a basic pathway of inoculation for theinfection in insect cuticle. Sometimes due to unfavourableconditions, the spore remain alive as mummified internallyinside the host cadaver for a long time and germinate asconditions become favourable31. It releases in theenvironment or in the field when insect cadavers break down.This behaviour makes them more suitable for large scale insectcontrol33.Most of the Entomopathogenic fungi are able to cause

epizootic disease in the insect population. Epizootic mean as“unusually large number of cases of disease" in a hostpopulation34 the prevalence of fungal infection in insect hostis similar to that of other organisms. However epizooticdisease development depends on host susceptibility,population and spreads efficacy through the contact betweeninfected hosts to a healthy one14,35. The horizontaltransmission maybe accorded form one host to another36,37

the behaviour of horizontal transmission is mostly found inhyphomycete fungi, the horizontal transmission was reportedin many insects such as; aphid, grasshoppers, locusts andDiaphorina citri. A high rate of host population increases thechances of contact among individuals and cause pathogentransmission, because overpopulation increases the stress andfungal infection38,39 (Fig. 1).

CHARACTERISTICS INVOLVING ININFECTION PROCESSES

Unlike other pathogens that required to be ingested,insect pathogenic fungi directly penetrate in the host cuticle40.The complex infectious process involved mechanicalincursion, while exhibiting different extracellular enzymes,which are responsible post-infection41-43. As the insect cuticlecontains up to 70% of protein, the penetration process isfacilitated by extracellular fungal proteases like subtilisins,chymotrypsins, trypsins and metalloproteases, usually withmultiple isoforms of each. Toxic metabolites with insecticidaleffect include substances as; beauvericins, isarolides,bassianolides, beauverolides, oosporein produced byBeauveria species or Isaria fumosorosea4,5. These substancesfacilitate to kill many different species of insect pests andarthropods, their capacity to facilitate penetrate into insectcuticle due this they become able to breakdown immunesystem of insects44. The insects killed infection coming intocontact spray droplets on its body, through walking on treatedarea or by feeding plants treated with the mycoinsecticidesonce the pathogenic conidia attached to the target host skin,they develop hyphae which penetrate into the insect’s cuticleand start multiplication45. Susceptible host cuticle componentsplay a dietetic role for the development of the conidial germtube depends on fungal species. After penetration, the fungusgerminates and multiplies inside the host insect haemocoel.The infected insect host usually killed 3-14 days afterpenetration of germ tube. However, sometimes it takes longer

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Temperature

Humidity

Abiotic factors

Rain

Dew drops

Irrigation

Solar radiation Successful infection

Leaf trichomes

Microbial interaction

Leaf size and shape

Crop structure

Host-plant quality

Biotic factors

Environmentalfactors

Fig. 2: Infection and disease development cycle

Fig. 3: Biotic and abiotic factors involves in infection and in disease development processes

time because of fungal intrinsic potential, the number ofconidia applied on targeted host species and onenvironmental condition as well15,46,47 (Fig. 2).

FACTORS INVOLVES IN INFECTION PROCESSES

Biotic factors: The host-plant chemistry plays an importantfactor which directly affects fungal infection, by suppressionor enhancing the conidial germination or via the insect,influencing its susceptibility or its development rate48,49.Plant quality, leaf structure, shape and leaf trichomes and

microbial interactions are also important factors22,50. Host-

specific is common in almost all entomopathogenic-fungi(Table 1) due to specific host characteristics these fungi onlyeffects on target insect pest and no direct effect on otherbeneficial insects i.e., parasites and predators. Though, nosignificant relationship was founded in the virulence of fungiother than its original host insect51,52, however, in some casesstudies showed that the repeated mass production of thesame species on artificial medium loss the virulence due tochanges in physiological and developmental process offungi53. The pose influence on the pathogenicity of fungidirectly either enhancing or by inhibiting conidial germinationon insect cuticle48,49 (Fig. 3).

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External fungal growth on cadaver and production of spores, released into environment

Germination on insect cuticle and penitration

Fungal spore coming into contact with an insect through spray droplets or by moving

Internal growth causing death of insect through physical organs deamage or production of toxic compounds

Infection process and disease cycle of entomopathogenic fungi

J. Entomol., 17 (2): 74-83, 2020

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Table 1: Pathogenicity level of different entomopathogenic fungi against various insect pests at different environmental conditions

Relative

Condition

Fungal species/strain

Target insect (Life stage)

Temperature (EC)

humidity (%)

Conidia/mL or mm2

Results (mortality %)

(Lab/Field)

References

I. fumosorosea Ifu-13a

Aphis gossypii Glover (Adult)

27.3-19.3

781×107/mL

95% mortality

Field

Bugti et al.63

B. bassiana strain Bb-202

91% mortality


Bemisia tabaci (Adult)

27.3-19.3

781×107/mL

41.6% insect population

Glasshouse

Bugti et al.64

declined

condition

B. bassiana strain Bb -202

Myzus persicae Sulzer (Adult)

21±1

78±5

6.75×105 conidia/mm2

100% mortality

Lab

Bugti et al.15

Jacobiasca formosana Paoli

21±1

78±5


97.4% mortality

Lab


21±1

78±5


81% mortality

Lab

Stephanitis nashi (Adult)

21±1

78±5


63.7% mortality

Lab

I. fumosorosea strain (Ifu13a)

Aphis gossypii (Adult)

21±1

78±5

1×108/mL

100% mortality

Lab

Bugti et al.65

Jacobiasca formosana (Adult)

21±1

78±5

1×108/mL

100% mortality

Lab


21±1

78±5

1×108/mL

100% mortality

Lab


21±1

78±5

1×108/mL

81% mortality

Lab

I. fumosorosea strain Ifu13a

Aphis gossypii (Adult)

21±1

78±5

1×108/mL

100% mortality

Lab

Bugti et al.52

Tinocallis kahawaluokalani (Adult)

21±1

78±5

1×108/mL

84% mortality

Lab

Aphis spiraecola (Adult)

21±1

78±5

1×108/mL

63.8% mortality

Lab

B. bassiana strain HQ-917687

Housefly (Adult)

3090-100

1×108/mL

100% mortality

Lab

Mishra et al.66

Housefly larvae

3070

1×108/mL

30-74% mortality

Lab

M. anisopliae

Ephestia kuehniella Zeller (Larvae)

25

558×1010/mL

93.9% mortality

Lab

Athanassiou et al.67

B. bassiana strain SZ-26

Frankliniella occidentalis (Adult)

25±1

60-70

1.6×107/mL

96% mortality

Lab

Wu et al.68


Nilaparvata lugens (Adult)

25±1

801×108/mL

35.1% mortality

Lab

Li et al.69


Nilaparvata lugen (Adult)

25±1

801×108/mL

20.2% mortality

Lab



25±1

801×108/mL

22.8% mortality

Lab



25±1

801×108/mL

17.2% mortality

Lab

B. bassiana strain Bb-r63


25±1

801×108/mL

42.8% mortality

Lab

B. bassiana strain Bb-r75


25±1

801×108/mL

27.9 % mortality

Lab

M. anisopliae strain Ma-12


25±1

801×108/mL

33.9 % mortality

Lab

Li et al.69



25±1

801×108/mL

65.4% mortality

Lab



25±1

801×108/mL

41.6% mortality

Lab

M. anisopliae strain (Ma-53)


25±1

801×108/mL

42.8 % mortality

Lab

M. anisopliae strain (Mf-19)


25±1

801×108/mL

49.3% mortality

Lab

M. anisopliae strain (Mf-82)


25±1

801×108/mL

82.1% mortality

Lab



2568.86

1.0×107/mL

47.03% mortality

Lab

Bai et al.46



2575.29

1.0×107/mL

81.14% mortality

Lab



2584.34

1.0×107/mL

100% mortality

Lab



2593.58

1.0×107/mL

100% mortality

Lab


Locusta migratoriamanilensis (Adult)

2568.86

1.0×107/mL

47.2% mortality

Lab



2575.29

1.0×107/mL

76.1% mortality

Lab

Bai et al.46



2584.34

1.0×107/mL

100% mortality

Lab



2593.58

1.0×107/mL

100% mortality

Lab



2295

1.0×107/mL

63.3% mortality

Lab



2595

1.0×107/mL

100% mortality

Lab



2895

1.0×107/mL

100% mortality

Lab



3195

1.0×107/mL

72.1% mortality

Lab



2295

1.0×107/mL

75% mortality

Lab



2595

1.0×107/mL

100% mortality

Lab



2895

1.0×107/mL

100% mortality

Lab



3195

1.0×107/mL

70 % mortality

Lab

P. fumosoroseus strain ARS EF 3594 b

Bemisia argentifolii (Nymphs)

23±2

49-54

1×103/mm2

55.8% mortality

Lab

Wraight et al.62

P. fumosoroseus Mycotech 613 b


23±2

25-30

1×103/mm2

36.2% mortality

Lab

B. bassiana ARS EF 252 b


23±2

49-54

1×103/mm2

73.6% mortality

Lab

B. bassiana ARSEF252


23±2

25-30

1×103/mm2

34.7% mortality

Lab

J. Entomol., 17 (2): 74-83, 2020

79

Table 1: Continue

Relative

Condition

Fungal species/strain

Target insect (Life stage)

Temperature (EC)

humidity (%)

Conidia/mL or mm2

Results (mortality %)

(Lab/Field)

References

B. bassiana Isolate GHA (Bb)


Temp: (16.5-26.1)

58.4-94.9

5.3×1013/mL

96.3% insect reduction

Field

Mean temp: 20.9

P. fumosoroseus Isolate 612 (Pfr)


Temp: (16.5-26.1)

RH (58.4-94.9)

5.3 1013/mL

98.8% insect reduction

Field

Mean temp: 20.9

mean 79.1% RH

B. bassiana CEP 332

Hedypathes betulinus (Adult))

26±1

70 RH

1×108/mL

61.8 % mortality

Lab

Schapovaloff et al.70

B. bassiana CEP 333

Hedypathes betulinus (Adult)

26±1

70 RH

1×108/mL

64.8% mortality

Lab

B. bassiana CEP 334


26±1

70 RH

1×108/mL

86.3% mortality

Lab

B. bassiana CEP 335


26±1

70 RH

1×108/mL

85.5% mortality

Lab


B. bassiana CEP 336


26±1

70 RH

1×108/mL

78.5% mortality

Lab

B. bassiana CEP 337


26±1

70 RH

1×108/mL

64.8% mortality

Lab

B. bassiana CEP 338


26±1

70 RH

1×108/mL

82.9% mortality

Lab

B. bassiana CEP 339


26±1

70 RH

1×108/mL

83.3 % mortality

Lab

B. bassiana CEP 340


26±1

70 RH

1×108/mL

68.5 % mortality

Lab

B. bassiana CEP 341


26±1

70 RH

1×108/mL

65.2% mortality

Lab

B. bassiana CEP 342


26±1

70 RH

1×108/mL

68.1% mortality

Lab

B. bassiana CEP 343


26±1

70 RH

1×108/mL

72.6 % mortality

Lab

B. bassiana CEP 344


26±1

70 RH

1×108/mL

68.5 % mortality

Lab

B. bassiana CEP 345


26±1

70 RH

1×108/mL

68.9% mortality

Lab

B. bassiana CEP 347


26±1

70 RH

1×108/mL

51.1 % mortality

Lab


M. anisopliae CEP 349


26±1

70 RH

1×108/mL

69.6% mortality

Lab

M. anisopliae CEP 350


26±1

70 RH

1×108/mL

81.8% mortality

lab

P. lilacinum CEP 352


26±1

70 RH

1×108/mL

0.0 % mortality

lab

P. lilacinum CEP 353


26±1

70 RH

1×108/mL

0.0% mortality

lab

B. bassiana

Aleurodicus dispersus

22.0-32.3

75-85.0 RH

2×109/mL

51.1% mortality

Field

Boopathi et al.71

M. anisopliae


22.0-32.3

75-85.0 RH

2×109/mL

45.4% mortality

Field

L. lecanii

Aleurodicus disperses

22.0-32.3

75-85.0 RH

2×109/mL

54.4% mortality

Field

I. fumosorosea


22.0-32.3

75-85.0 RH

2×109/mL

59.1% mortality

Field

B. bassiana MBC 076

Aedesaegypti

28<C

70-80

1×108/mL

94.9% mortality

Lab

Ramirez et al.72

L. lecanii strain V3.4504

Matsucoccus matsumurae (Kuwana) 2nd instar

25±0.5

75±10 RH

5×107/mL

53.6% mortality

Lab

Liu et al.73



25±0.5

75±10 RH

5×107/mL

61.3% mortality

Lab

F. incarnatum-equiseti strain HEB01


25±0.5

75±10 RH

5×107/mL

40.3% mortality

Lab

L. fungicola strain HEB02

Matsucoccus matsumurae (Kuwana) 2nd instar larvae

25±0.5

75±10 RH

5×107/mL

32.7% mortality

Lab


Matsucoccus matsumurae (Kuwana) (Adult)

25±0.5

75±10 RH

5×107/mL

86% mortality

Lab


Matsucoccus matsumurae (Kuwana)

25±0.5

75±10 RH

5×107/mL

100% mortality

Lab

F. incarnatum-equiseti Strain HEB01


25±0.5

75±10 RH

5×107/mL

83% mortality

Lab

L. fungicola strain HEB02


25±0.5

75±10 RH

5×107/mL

41.3% mortality

Lab

Liu et al.73

B. bassiana Bb-01

Musca domestica (Adult)

27±1

>75 RH

3×108/mL

86% mortality

Lab

Farooq and Freed74

B. bassiana Bb-10


27±1

>75 RH

3×108/mL

68% mortality

Lab

M. anisopliae Ma-2.3


27±1

>75 RH

3×108/mL

78% mortality

Lab

M. anisopliae Ma-11.1


27±1

>75 RH

3×108/mL

61% mortality

Lab

I. fumosorosea If-02


27±1

>75 RH

3×108/mL

56% mortality

Lab

I. fumosorosea If-2.3


27±1

>75 RH

3×108/mL

68% mortality

Lab

B. bassiana 6884

Rhynchophorus ferrugineus (larvae)

30±1

75±5 RH

1×107/mL

100% mortality

Lab

Hussain et al.75

I. fumosorosea 9602


30±1

75±5 RH

1×107/mL

96.8% mortality

Lab

M. anisopliae 9H755


30±1

75±5 RH

1×107/mL

56% mortality

Lab

J. Entomol., 17 (2): 74-83, 2020

Abiotic factors: Suitable environmental factors i.e.,temperature and relative humidity play an important role indisease development and infection process of fungi54,55.Humidity is more important than temperature, which posesgreat influence on the inducing fungal disease in the host53 ,56.However, literature showed that 50% relative humidity alsohelpful infection process in some cases46,57. High humidityhelps conidia to penetrate in the target host (Table 1).It is reported58 that the relative humidity provides better

results as compare than temperature in the glasshouses mostof insect-pathogenic fungi grow and sporulate at optimumtemperature ranged from 15-30EC46,59. The ideal range oftemperature for greatly enhances the growth and rapidinfection, though germination of conidia retarded thedevelopmental process of host insect. However, many insectsescape from fungal infection by molting60, 61. That’s why mostof the entomopathogenic fungi fail to induce fungal diseasein earlier larval stage62 (Table 1).

CONCLUSION AND RECOMMENDATIONS

It was concluded from previous literature that higherfungal conidial density provides rapid and better control. Thestudy also showed that most of the fungi are host-specific.Moreover, host-specificity is not related to phylogeneticrelationship. This was observed that initial infection is themost critical stage of causing an epizootic disease, once fungibuilt a successful infection in targeted insect population, itsharply spread and kills their hosts. Study further revealed thatthe virulence of entomopathogenic fungi significantly affectedby biotic and abiotic factors such as; fungal species, host plantchemistry, insect host and its life stages and temperature,sunlight and relative humidity, respectively. Among thesefactors, the relative humidity seems to be more importantthan other factors to ensure infection and successful diseasedevelopment in targeted insect population. The farmers/horticulturists from the coastal areas with

high relative humidity over than 60% with moderatetemperature are strongly advised to use conidia base myco-insecticides for insect control to limit excessive application ofchemical pesticides and make sure a healthy environment.

SIGNIFICANCE STATEMENT

This review article will help the researcher to understandvarious factors, which are involved in causing infection andsuccessful disease development in many insect pests. This

review also provides information about effective range oftemperature and humidity of different Entomopathogenicfungal species to manage the insect pest infestation.

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