BIOLOGICAL CONTROL OF HEMIPTERAN PESTS

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Biological Control of Hemipteran Insects
Mandeep Rathee Ph. D. Entomology, CCSHAU, HISAR
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Biological control
Biological control usually refers to the action
of parasites, predators or pathogens on a pest
population which reduces its numbers below a
level causing economic injury.
Cyclic relationship between a biocontrol agent
and its host or prey (pest)
Methods
1. Importation 2. Augmentation 3. Conservation
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Order Hemiptera

• Predominant feature - Piercing-sucking
  mouthparts.
• Hemipterans are omnivores, alternating between a
  plant-based and an animal-based diet.
• Some species are important agricultural pests
  damaging crops by the direct action of sucking
  sap like red cotton bug, but also harming them
  indirectly by being the vectors of serious viral
  diseases such as whiteflies, aphids.
• Members of the families Reduviidae and Nabidae are
  obligate predators. Some predatory species are
  used in biological pest control these include
  various nabids and even some members of families
  that are primarily phytophagous, such as the
  genus Geocoris in the family Lygaeidae.

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Agricultural Important Insects
S. No Name of the insect Common name Order Family
1 Aleurocanthus woglumi Ashby Citrus black fly Hemiptera Aleyrodidae
2 Bemisia tabaci (Gennadius) Tobacco whitefly, cotton whitefly Hemiptera Aleyrodidae
3 Dialeurodes citri (Ashmead) Citrus whitefly Hemiptera Aleyrodidae
4 Aphis craccivora Koch Cowpea aphid Hemiptera Aphididae
5 Eriosoma lanigerum (Hausmann) Woolly apple aphid Hemiptera Aphididae
6 Liaphis erysimi (Kaltenbach) Turnip aphid Hemiptera Aphididae
7 Myzus nicotina Blackman Green peach aphid Hemiptera Aphididae
8 Myzus persicae (Sulzer) Green peach aphid Hemiptera Aphididae
9 Coccus viridis (Green) Green scale Hemiptera Coccidae
10 Aonidiella aurantii (Maskell) California red scale Hemiptera Diaspididae
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11 Chrysomphalus aonidum (Linnaeus) Black scale Hemiptera Diaspididae
12 Lepidosaphes beckii (Newman) Purple scale Hemiptera Diaspididae
13 Melanospis glomerata (Green) Sugarcane scale, Black Araucaria scale Hemiptera Diaspididae
14 Quadraspidiotus perniciosus (Comstock) San Jose Scale Hemiptera Diaspididae
15 Pyrilla perpusilla (Walker) Indian sugarcane leafhopper Hemiptera Lophophidae
16 Maconellicoccus hirsutus Green Pink Hibiscus mealy bug Hemiptera Pseudococcidae
17 Planococcus citri (Risso) Citrus mealy bug Hemiptera Pseudococcidae
18 Planococcus lilacinus (Cokerell) Coffee mealy bug Hemiptera Pseudococcidae
19 Heteropsylla cubana Crawford Subabul psyllid, leucaena psyllid Hemiptera Psyllidae
20 Antilochus coqueberti (Fabricius) Pyrrhocorid bug Hemiptera Pyrrhocoridae
21 Dysdercus cingulatus (Fabricius) Red cotton bug Hemiptera Pyrrhocoridae
22 Stephanitis typicus (Distant) Coconut lace wing bug, Banana lace wing bug Hemiptera Tingidae
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Major predators of Hemiptera order
S. No Name of the insect Category Order Family
1 Anthocoris minki Dhorn Predator of Psyllids Hemiptera Anthocoridae
2. Rhynocoris fuscipes (Fabricius) Predator of aphids, nymphs, eggs and immature stages Hemiptera Reduviidae
3. Rhynocoris marginatus (Fabricius) Predator of aphids, nymphs, eggs and immature stages Hemiptera Reduviidae
4. Cyrtorhinus lividipennis Reuter Predator of nymphs and adults of brown plant hopper partly plant feeder Hemiptera Miridae
5. Stethoconus praefectus (Distant) Predator on Avacado Lace bug Hemiptera Miridae
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LANDMARK EXAMPLES IN CLASSICAL BIOLOGICAL CONTROL
Insect Natural enemy Year of importation From country To country
cottony cushion scale, Icerya purchasi coccinellid, Rodolia cardinalis 1888 Australia California (McLeod, 1939)
Greenhouse Whitefly, Trialeurodes vaporariorum aphelinid parasite Encarsia formosa 1933-1934 Tropical America Australia (Clausen, 1978), (McLeod, 1939)
Southern Green Stink Bug, Nezara viridula egg parasite Trissolcus basalis 1933 Egypt Australia (Clausen, 1978)
Citrus blackfly, Aleurocanthus woglumi Prospaltella smithi, P. clypealis, P. opulenta, Amitus hesperidum and Eretmocerus serius 1949-1950 Pakistan and western India Mexico (Shaw, 1950).
Spotted alfalfa aphid, Terioaphis trifolii aphidiids Praon exsoletum, Trioxys complanatus and the aphelinid Aphelinus asychis 1959 New Mexico California (Van den Bosch, 1959)
California red scale, Aonidiella aurantii ectoparasites Aphytis chrysomphali, A. lignanensis, A. melinus, endoparasites Prospallella perniciosi 1902 1947 1956 1949 China, India, Taiwan and southern China California (Van den Bosch and Haramoto, 1953)
San Jose scale, Quadraspidiotus perniciosus Prospaltella perniciosi 1947 California USSR (Mathys, 1966)
(Caltagirone, 1981)
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Successful Examples of CBC in India
1. Cottony Cushion Scale, Icerya purchasi Maskell
(Margarodidae)
Icerya purchasi (Origin Australia) was probably
introduced on imported orchard stock or flowering
plants from Sri Lanka and it spread to cultivated
wattles, rose-bushes and citrus. It was first
reported from Nilgiris (Tamil Nadu) in 1928 as a
pest of cultivated wattle, Acacia decurrens and
other Acacia spp. The coccinellid beetle,
Rodolia cardinalis (Origin Australia), was
introduced to India in 1926 via USA (California)
and South Africa and in 1930 via Egypt for the
control of I. purchasi. The beetle was released
in the Nilgiris in 1930 and it successfully
controlled I. purchasi.
2. Mealybugs
Common mealybug (Planococcus citri), grape
mealybug (Maconellicoccus hirsutus), mango
mealybug (Rastrococcus iceryoides ), spherical
mealybug (Nipaecoccus viridis ), striped mealybug
(Ferrisia virgata), oriental mealybug
(Planococcus lilacinus,) and pineapple mealybug
(Dysmicoccus brevipes) are hard to kill pests
not affected by foliar application of
insecticides since they are covered with waxy
coating.
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The first intentionally introduction was the
coccinellid predator, Cryptolaemus montrouzieri
which was introduced in June 1898 by Mr. H.O.
Newport, an amateur entomologist and coffee
planter of Palni hills (Tamil Nadu). Eight
commercial insectaries are supplying C.
montrouzieri to the growers. Biocontrol Research
Laboratory of Pest Control India (P.) Ltd.
established in Bangalore in 1981, has been
producing and supplying this predator since
inception.
3. Common Mealybug, Planococcus citri (Risso)
(Pseudococcidae)
Planococcus citri was described from citrus in
southern France. In India, it is a pest of
citrus, coffee, passion fruit, cut flowers and
many other fruit crops and wild plants. this pest
prefers to feed on the fruit stalk or on the
berries resulting in their drop. The encyrtid
parasitoid Leptomastix dactylopii (Origin
Brazil) was introduced into India in 1983 from
Trinidad, West Indies. It is capable of
parasitising Planococcus citri and P. lilacinus.
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4. San Jose Scale, Quadraspidiotus perniciosus
(Comstock) (Diaspididae)
Quadraspidiotus perniciosus is a polyphagous pest
of Oriental origin. It is a serious pest of apple
in north-western India. It also attacks other
deciduous trees, poplars and willows. Aphelinid
parasitoid Encarsia perniciosi (Origin Far East)
strain from California was introduced in 1958 and
Illinois, Chinese and Russian strains were
introduced in 1960 for the biological suppression
of San Jose scale. Russian strain gave 89 per
cent parasitism in Himachal Pradesh.
5. Woolly Aphid, Eriosoma lanigerum (Hausmann)
(Aphididae)
Eriosoma lanigerum is a native of Eastern United
States. It was probably accidentally introduced
to India from England as indicated from its
record in Shimla district of Himachal Pradesh
where nursery stocks were imported. For the
control of woolly aphid, exotic aphelinid
parasitoid, Aphelinus mali, a native of North
America, was introduced from UK at Saharanpur
(Uttar Pradesh). The parasitoid could control
woolly aphid in Kullu valley (Himachal Pradesh)
and has spread to Kashmir valley.
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6. Spiralling Whitefly, Aleurodicus dispersus
Russell (Aleyrodidae)
Spiralling whitefly, Aleurodicus dispersus, was
first reported from Kerala in 1995. It causes
serious damage to avocado, banana, cassava,
guava, papaya and mango, besides sevaral
ornamental trees. Exotic aphelinid parasitoids,
Encarsia guadeloupae (Origin Carribbean
region/Central America) collected from Minicoy
Island of Lakshadweep and brought to main land
have established well, causing perceptible
reduction in pest population. Parasitism levels
due to both parasitoids vary from 29-70 and
exceed 90 during some parts of the year.
7. Subabul Psyllid, Heteropsylla cubana Crawford
(Psyllidae)
Subabul, Leucaena leucocephala was introduced
into India for cattle feed and fuel for use of
the rural population. Leucaena psyllid
Heteropsylla cubana, a native of South America
invaded subabul in 1988. It devastated subabul
plantations in Karnataka, Kerala, Tamil Nadu and
Andhra Pradesh. The coccinellid predator,
Curinus coeruleus (origin South America) was
obtained from Thailand in 1988 for the biological
suppression of H. cubana.
Singh, 2004
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Case study 1. Natural parasitization of
sugarcane leaf hopper, Pyrilla perpusilla (Walk.)
in Uttarakhand
The experiment was conducted at Crop Research
Center of GBPAUT, Pantnagar. The maximum number
of egg mass, nymph and adult per leaf of pyrilla
observed was 6.67, 22.67 and 18.00 on 30th ,
30th and 15th August, respectively. The highest
parasitization of eggs masses by Tetrastichus
pyrillae was observed in the month of October
i.e. 85.33 indicating peak activity of
parasitoid. The maximum population of egg, pupa
and adult/ leaf of E. melanoleuca were 8.00,
18.67 and 27.33 on 30th Sept., 15th of Oct. and
30th Oct., respectively.
,
(Kumar et al., 2008)
Case study 2 Natural enemies of Pyrilla
perpusilla Wlk. in Northern Pakistan
The experiment was conduct in sprayed areas of
Mardan and unsprayed areas of Tordher in
Pakistan. Results revealed that maximum
population of predator, Epipyrops melanolecua
Fletcher was found during month of October at
Tordher and in November at Mardan. Other
predators viz., Coccinella septumpunctata, C.
undecimpunctata, Menochilus sexmaculatus and
Brumus suturalis found in low no. and no
significant difference observed in sprayed and
unsprayed fields. The parasite, Ooenocyrtus
papillionis Ashm. incidence was 9, 8 and 12 per
cent during sept., Oct. and Nov., respectively in
sprayed areas whereas in unsprayed field
corresponding figures were 10, 19 and 33 per
cent. It showed highest incidence during November.
(Irshad and Mirza, 1982)
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Case study 3 Biological control of the sugarcane
woolly aphid (Ceratovacuna lanigera) in Indian
sugarcane through the release of predators Dipha
aphidivora Meyrick (Lepidoptera Pyralidae),
Micromus igorotus Bank (Neuroptera Hemerobiidae)
and Eupeodus confractor Wiedemann (Diptera
Syrphidae)
During 200304, 200405 and 2005-06, 49.23 ,
76.25 and 77.87 control was achieved through
predation, respectively. Release of predators at
2500 larvae and/or cocoons per ha effectively
controlled the SWA.
(Patil et al. 2007)
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Case study 4 Preliminary studies on field
parasitization and biology of solenopsis mealybug
parasitoid, Aenasius bambawalei Hayat
(EncyrtidaeHymenoptera).
(Ram et al., 2009)
Case study 5. Population trends of Aenasius
bambawalei Hayat and its role in controlling
mealy bug Phencoccus solenopsis Tinsley at
Tandojam Sindh
Host Plant Parasitism percent Abutilon indicum
94 Cotton 93 Okra 91 Sunflower
90 Rose of China 89 Datura 88 Egg
plant 87 Withania somnifera 55
(Solangi and Mahmood, 2010)
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Population trends of mealy bug and parasitoid
Aenasius bambawalei on Abutilon indicum
Population trends of mealy bug and parasitoid
Aenasius bambawalei on cotton
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Case study 6 Papaya mealybug and its biological
control
1. Parasitoids introduced in India for management
of papaya mealybug
Order Family Species Reference
Hymenoptera encrytidae Acerophagus papayae
Jothi et al. (2011) Hymenoptera encrytidae
Anagyrus loecki (Noyes) Nakata et al.(2011)
Hymenoptera encrytidae Pseudleptomastrix
mexicana Nakata et al.(2011)
2. Predator reported from India
Order Family Species Reference
Lepidoptera Lycaenidae Spalgis epius
(Westwood) Krishnamurthy and Mani (2011).
Coleoptera Coccinellidae Cryptolaemus
montrouzieri Jonathan et al. (2011)
Coleoptera Coccinellidae Scymnus
taiwanus (Ohta) Nakata et al. (2011)
Coleoptera Coccinellidae Cheilomenus
sexmaculatus Jonathan et al. (2011)
Coleoptera Coccinellidae Coccinella
transversalis Jonathan et al. (2011)
Neuroptera Chrysopidae Chrysoperla
carnea Ayyasamy and Ragupathy (2010)
Diptera Syrphidae Ischiodon
scutellaris Shylesha et al. (2011)
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3. Entomopathogenic fungi
Entomopathogenic fungi Reference Metarrhizum
anisopliae (Metsch.) Shylesha et al., 2010
Verticillium lecani (Zimm.) Mani Chellappan,
2011 Paecilomyces pictus Ayyasamy and
Ragupathy, 2010 Beauveria bassiana (Bals.)
Shylesha et al., 2010 Neozygyites Chilocorus
nigrata Fab Shylesha et al., 2010
Parasitoid State Plants Year Reduction in
pest population A. papayae kerala
Rubber, Plantation crops 2011 80 A. papayae
Odisha Agricultural crops 2011 70-80 A.
papayae Bangalore Jatropha 2010 80-90 A.
papayae Maharashtra Papaya 2010 85-92 A.
papayae Tripura Papaya 2009-10 60
Among the parasitoids released, the highest
proliferation and field activity was observed in
the case of A. papayae, which accounted for 75.6
81.7 parasitization followed by P. mexicana
(9.3-24.4) whereas A. loecki registered
comparatively very poor performance (0.7- 9.0 )
(Dey, 2016)
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Case study 7 Biological control of rice
leafhoppers and planthoppers in Andhra Pradesh
The study resulted that the mymarid Anagrus sp.
and the trichogrammatid Oligosita sp. are the
most common egg parasitoids of Nilaparvata
lugens, while another mymarid, Gonatocerus sp.,
and another trichogrammatid, Paracentrobia sp.,
attack eggs of Nephotettix virescens and N.
nigropictus. Among the predators, the mirid
bug Cyrtorhinus lividipennis and Coccinella
arcuata prey on Nilaparvata lugens. The main
pathogens infecting these pests include Beauveria
bassiana, which attacks Nephotettix
virescens and N. nigropictus during
September-November, and Entomophthora fumosa,
which infects Nilaparvata lugens during September.
Gupta and Pawar, 1989
Case study 8 Bioefficacy of Beauveria bassiana
and Paecilomyces amoeneroseus against rice green
leaf hopper
Effect of 22 h of feeding access of leafhoppers
on membrane sachet (containing spores suspension
10 sucrose solution) on survival of
Nephotettix virescens
Fungi Mortality Beauveria bassiana 95 Paecil
omyces amoeneroseus 20 Control No mortality
(Niazi et al., 2002)
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Case Study 9 Efficacy of some entomopthogenic
fungi against brown plant hopper, Nilaparvata
lugens Stal in irrigated rice
Adult
Eggs
Nymphs
(Reddy et al., 2013)
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Cumulative mean effect of entomopathogenic fungi
on C. lividipennis and spiders
Wolf spider, Pardosa pseudoannulata
Mirid bug
(Reddy et al., 2013)
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Case study 10. Effectiveness of leafhopper
control varies with lacewing release methods
Average leafhopper densities found in lacewing
release and no release plots in three Thompson
seedless vineyards in (A) 1991 anwe) 1992. C.
carnea eggs were released a approximately
3,500/acre in the first brood and 7,000acre in
the second brood.
Lacewing eggs were mixed with corn grit and
placed in 5-gallon containers
Studies in experimental plots and commercial
vineyards showed that releases of green lacewings
at rates between 3,000 and 8,000 per acre for
each variegated grape leafhopper, Erythroneura
variabilis brood (costing 9 to 24 per acre for
each brood) reduced leafhopper densities up to
35.
(Daane et al., 1993)
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Case study 11. Effects of different management
schedules on parasitization of whitefly pupae by
Encarsia sp.
The experiment was conducted on pupal
parasitization of whitefly by Encasrsia sp. on
cotton crop at CCSHAU, Hisar. The results
revealed that maximum pupal parasitization with
74.79 per cent was observed in S2 (Plants sprayed
with nimbecidine at 5 days interval yellow
sticky trap) followed by 70.82 per cent in S1
(plants sprayed with nimbecidine at 5 days
interval) which was significantly at par with
(untreated control).
(Mehra and Rolania, 2015)
Encarsia species and Eretmocerus mundus are
important parasitoids for control of the
greenhouse whitefly, Trialeurodus vaporarium
(Van Lenteren, 1986), ash whitefly (En. inaron)
(Gould et al., 1992) and citrus whitefly (En.
lahorensis) (Argov, 1986). Recently, additional
Encarsia species have been included in biological
control efforts in California using En.
protransvena and En. sophia (transvena) against
B.tabaci and En. variegata against citrus
whitefly.
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Case study 12. Development of Encarsia bimaculata
(Heraty and Polaszek) (Hymenoptera Aphelinidae)
in Bemisia tabaci (Gennadius) (Homoptera
Aleyrodidae) nymphs
female laying egg
female egg
ovipositional puncturing
second instar, exuviae
extraembryonic membrane
first instar tail
third instar larva, S spiracle L, ileolabial
gland
prepupa laying meconium
virgin female laying unfertilized egg
on E. bimaculata female third instar
on E. transvena female prepupa,
on E. bimaculata female early black pupa
(Antony et al., 2004)
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First instar
Male egg on third instar
Male egg on prepupa
Second instar
Third instar
Third instar consumes the host
Black pupa
Adult E. bimaculata prior to emergence
Prepupa
Male and female E. bimaculata
E. bimaculata black pupa
Hyperparasitized male again parasitized by
another E. bimaculata
(Antony et al., 2004)
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Case study 13. Evaluation of Three Different
Insect Pathogenic Fungi for the Control of
Dysdercus koenigii and Oxycarenus hyalinipennis

• Virulence of three different entomopathogenic
  fungi i.e., B. bassiana, Isaria fumosorosea and
  M. anisopliae were evaluated against the adults
  of red cotton bug.
• Cumulative percentage mortality of B. bassiana,
  I. fumosorosea and M. anisopliae on red cotton
  bug were 95.00, 70.00 and 80.00 respectively over
  a period of 7 days at the concentrations of 3108
  spores/ml.
• B. bassiana with lowest LC50 value of 2.5107
  spores/ml and LT50 of 4.32 days proved to be most
  virulent isolate against dusky cotton bug as
  compared to I. fumosorosea with 8.5107 spores/ml
  and M. anisopliae 8.1107 spores/ml.
• Accumulative percentage mortality of these three
  insect killing fungi, B. bassiana, I. fumosorosea
  and M. anisopliae on dusky cotton bug were 90.00,
  75.00 and 75.00, respectively over a period of 7
  days at the concentrations of 3108 spores/ml.

(Khan et al., 2010)
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Case study 14. Management of an Invasive Stink
Bug, Bagrada hilaris - a review

• Most are egg parasitoids belongs to family
  Platygastridae and include several species in the
  genera Telenomus, Paratelenomus, Gryon sp.,
  Trissolcus (all formerly in the family
  Scelionidae) and Ooencyrtus (Encyrtidae).
• Field parasitism rates ranging from 15 to 25
  were reported for Telenomus on soil-borne eggs
  during March and April in India, but wasp numbers
  decreased in May. Higher parasitism (30) was
  recorded for eggs that were not covered by soil
  (Samuel, 1942).
• Laboratory parasitism rates of 22 for soil-borne
  eggs and 25 for eggs on the soil surface were
  reported for Typhodytes (Typhodytes sp.), but a
  parasitism rate of only 1820 was found in the
  field (Samuel, 1942). Ghosal (2006) reported a
  reduviid bug (Harpactor segmentarius Germ.)
  feeding on B. hilaris nymphs and adults.

(Palumbo et al., 2015)
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Fungi as a Biocontrol agent for the management of
Insect pests a review

• The fungi like Metarhiziun anisopliae (Metch.)
  Sorokin., Beuveria bassiana (Bals.) Vuillemin,
  and Lecanicillium lecanii (Zimm.) have gained the
  great scope as a biological control agents for
  the insect pest management. L. lecanii is one of
  the important entomopathogenic fungi, which was
  formerly known as Verticillium lecanii Zimm .
• The effectiveness of L. lecanii was studied and
  demonstrated first in India by Easwaramoorthy
  (1978). It is effective for the control of sap
  feeding pest like aphids, whiteflies, scale
  insects, thrips and mealy bugs.
• Kim et al. (2002) reported that lower
  concentration (1 x 103-107 conidia /ml) of fungus
  exhibited relatively low mortality in adult
  whitefly, Bemisia tabaci, while higher
  concentrations (109 and 108 conidia /ml)
  exhibited almost 100 mortality of B. tabaci,
  after 7 and 9 days of treatments under greenhouse
  conditions.

(Shinde et al., 2010)
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List of commercial products of L. lecanii,
(Shinde et al., 2010)
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Commercial Scale Production of Mycoinsecticides
in different countries
Beauveria Mycotrol Whiteflies/Aphids/Thrips
Field Crops Mycotech, USA bassiana
Naturalis Sucking insects cotton,
glasshouse crops Troy BioScience,
USA Metarhizium Bio Magic Brown plant hopper
Rice T. Stanes, India anisopliae Verticillum
Vertilec Aphids, Whiteflies
Glasshouse crops Koppert, Holland lecanii
Mycotal Inovert Aphids, Scales,
Mealybugs - Inora, India Biocatch
Whiteflies Cotton T. Stanes, India
Verticare Mealybugs Scales Citrus
Viswamitra Bio Agro,
India Paecelomyces PFR-97TM
Whiteflies/Thrips Glasshouse crops
Thermo Trilogy, fumosoroseus
USA
(Ramanujam et al., 2014)
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Biological Control of pests using
entomopathogenic fungi in India
(Ramanujam et al., 2014)
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Aphids
Entomophthorales fungus
Pandora neoaphidis (Remaudiere Hennebert)
Humber Zoophthora radicans (Brefeld)
Batko Neozygites fresenii (Nowakowski)
Batko Entomophthora planchoniana Cornu
sporulation
Epizootics of the entomophthoralean fungus
Pandora neoaphidis in an aphid population
Rhopalosiphum maidis sporulation of P. neoaphidis
on legs and antennaea
(Wraight et al., 2009)
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Leafhopper
Entomophthorales Fungus Causing Epizootics
Nymph of E. fabae killed by Z. radicans
Nymph of potato leafhopper, Empoasca fabae
infected with Zoophthora radicans
Adult E. kraemeri killed by Z. radicans (green
colouration of fresh fungal growth )
Fungal outgrowth from the host cadaver forms a
mat of specialized hyphae that actively discharge
infectious conidia
(Wraight et al., 2009)
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Conclusion

• Biological control is an eco-friendly approach
  and helpful in effective management of serious
  insect-pests of agricultural crops.
• There are several landmark examples in classical
  biological control in India as well as in other
  countries such as control of the cottony cushion
  scale, Icerya purchasi, in California with the
  predatory coccinellid, Rodolia cardinalis
  imported from Australia in 1888.
• In some cases, total reduction of a pest to a
  non-pest status has resulted in others, the
  impact of the beneficial species becomes the
  pivot around which a series of other procedures
  (integrated pest control) is organized and
  implemented.

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Thank you