Review Article
Biocontrol of agricultural pests
Chandrika Mohan and A. Josephrajkumar
ICAR-Central Plantation Crops Research Institute, Regional Station,
Kayamkulam, Kerala, India
Corresponding Author: Chandrika Mohan, E-mail: cmcpcri@gmail.com
Received: 06/08/2024; Revised: 12/10/2024; Accepted: 21/10/2024; Published: 29/01/2025
___________________________________________________________________________
Abstract
Biological control is an environmentally safe method used in integrated pest management. It involves
suppression of pest population using two groups of living organisms referred to as Entomophaga and
Entomopathogens. Entomophaga comprise natural predators and parasites of the pest. Entomopathogens are
generally microorganisms that include virus, bacteria, fungi, nematodes and protozoa. This review gives an
account of various biological control methods including ecological engineering and push-pull strategy with
examples and discusses the advantages as well as challenges associated with them.
Keywords: Biological control, Entomophaga, Entomopathogen, Ecological engineering, Push-Pull strategy.
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Introduction
The central core to the performance of many ecosystem processes is the insects which in their dominance and
long evolutionary background occupy every niche of the earth. Though many insects are beneficial to mankind,
some of them interfere with man and his properties aptly termed as “Pests” which could cause direct feeding
injury (red palm weevil) or serve as vectors transmitting diseases (Banana aphid transmitting bunchy top
disease). Biological control is one of the widely adopted tools in pest management programme that targets
environmental and ecological stability by holding biodiversity together. Biological control involves suppression
of pests using other living organism which includes two major categories such as (i) Entomophaga
encompassing predators and parasitoids and (ii) Enomopathogens involving virus, bacteria, fungi, nematodes,
protozoa etc.
Types of biological control
Biological control is one of the critical components of Integrated Pest Management programme and owing
allegiance to environmental and human safety, this approach formed the centre stage of sustainable pest
suppression these days. The word Biological controlwas first used by Prof. Harry Scott Smith during 1919;
however, its widespread usage was popularized by Prof. Paul H. Debach, a noted citrus entomologist. It could
be classical biological control where introduction of natural enemies is usually undertaken from the centre of
origin of the invasive pest through standard protocols and get systematically released in the new country of
infestation. E.g., Bio-suppression of papaya mealy bug (Paracoccus marginatus) in India through introduction
of the encyrtid parasitoid, Acerophagous papaya from Puerto Rico. Under augmentative biological control, it
could be either inoculative with one time release of natural enemies (E.g., Release of green lacewing,
Chrysoperla zastrowii sillemi for the bio-suppression of sucking pests [Hopper, Amrasca devastans; aphid,
Aphis gossypii] of cotton) or innundative with frequent release of natural enemies based on the pest incursion
status (E.g., Frequent release of stage-specific parasitoids, Goniozus nephantidis or Bracon brevicornisin the
bio-suppression of coconut black
.
headed caterpillar, Opisina arenosella). Though conservatory biological control is not so prominent and
successful in several cropping systems, its silent but significant role in the bio-suppression of two invasive
whiteflies, viz., spiralling whitefly (Aleurodicus dispersus Russell) and rugose spiraling whitefly (Aleurodicus
rugioperculatus Martin) by aphelinid parasitoids Encarsia dispersa and Encarsia guadeloupae is noteworthy.
Entomophaga
Predators
In general, predators kill the prey for itself and are usually larger than the prey. Predators are mainly free-living
species that directly consume a large number of preys during their whole lifetime. The first international
shipment of an insect as biological control agent was made by Charles V. Riley in 1873, delivering France the
predatory mites Tyroglyphus phylloxera to help fight the grapevine phylloxera (Daktulosphaira vitifoliae) that
was destroying grapevines in France. In 18881889 the vedalia beetle, Rodolia cardinalis, a lady beetle, was
introduced from Australia to California to control the cottony cushion scale, Icerya purchasi. This had become a
major problem for the newly developed citrus industry in California, but by the end of 1889 the cottony cushion
scale population had already declined, and this successful bio-suppression strategy is termed as Miracle of
Entomology”.
For rodent pests, cats are natural predators and hence, they can be employed for rodent control, in
conjunction with reduction of "harborage"/hiding locations. Barn owls are also sometimes used as biological
rodent control. Due to the absence of rat snakes and owls in Lakshadweep Islands, rats emerged as a major pest
of coconut, reducing yield by about 40%.
The red spot reduviid predator, Platymeris laevicolis imported from Zanzibar was found to be an excellent
predator of rhinoceros beetle, Oryctes rhinoceros (Figure 1a). A wide array of spiders is recorded as predators
of black headed caterpillar, Opisina arenosella of which Rhena, Sparassus and Cheiracanthium are the major
ones. Many predatory mites including Amblyseius largoensis, Neoseiulus paspalivorus and Bdella distincta
were reported as potential predators of coconut eriophyid mite, Aceria (Figures 1b and 1c).
Parasites and parasitoids
A parasite and its host belong to two different classes taxonomically and usually a parasite will never kill the
host but could cause extreme level of parasitism. For example, head louse on humans is a parasite. On the other
hand, parasitoid and the host belong to the same class and usually a parasitoid kills the host. The bethylid larval
parasitoid of Goniozus nephantidis parasitizes and kills the host, black headed caterpillar, O. arenosella (Figure
2a), while a predator kills the host for itself, and a parasitoid parasitizes the host for its progenies.
The stage specific parasitoids of O. arenosella viz., the larval parasitoids Goniozus nephantidis (Bethylidae),
Bracon brevicornis (Braconidae) (Figure 2b), the prepupal parasitoid, Elasmus nephantidis (Elasmidae), and
the pupal parasitoid Brachymeria nosatoi (Chalcididae) are the most promising ones which are extensively
used for augmentative releases for pest suppression (Figure 2c). The major desirable attributes of these
parasitoids are their greater host searching ability, production of higher proportion of females, occurrence
throughout the year and their distribution in all pest infested areas. A large area field validation of the bio-
suppression technology of
coconut black headed caterpillar with regular monitoring and release of stage specific parasitoids viz., G.
nephantidis, B.brevicornis, E. nephantidis and B. nosatoi was taken up during 1999-2002 in different
geographic locations in coastal Karnataka and Kerala comprising of a total of 1,400 ha could achieve 93-100 per
cent reduction in O. arenosella population in a period of two years. Very recently the natural bio-suppression of
the rugose spiralling whitefly, Aleurodicus rugioperculatus by the aphelinid parasitoid, Encarsia guadeloupa
(Figure 2d) is a classic example of conservatory biological control which could parasitize the pest to more than
85% in a pest prone area. In this backdrop, a pesticide holiday is advised for the natural buildup of the
parasitoid, E. guadeloupae.
Entomopathogens
This category includes microbial pathogens such as virus, bacteria, fungi, protozoa and nematodes used in
biological pest suppression. [1-6]
Virus
Insect viruses (baculovirus) are obligate disease-causing organisms that can only reproduce within a host insect.
They can provide safe, effective and sustainable control of a variety of insect pests, although they are most
effective as part of a diverse integrated pest management program. They are broadly classified as occluded or
non-occluded types based on the occlusion of virion particles. Virus infection begins in the insect’s digestive
system but spreads throughout the whole body of the host in fatal infections. The body tissues of virus-killed
insects are almost completely converted into virus particles. The digestive system is among the last internal
organ systems to be destroyed, so the insects usually continue to feed until they die.
The occluded viruses such as Spodoptera litura nuclear polyhedrosis virus, Helicoverpa armigera nuclear
polyhedrosis virus, Cydia pomonella granulosis virus are very effective and commercially used in biological
pest suppression. In coconut, the use of non-occluded virus, Oryctes rhinoceros nudivirus (OrNV) is very
effective and kills the O. rhinoceros grub in 15 -20 days’ time significantly suppressing the longevity and
fecundity of adult beetles (Figures 3a-c). OrNV was first reported from Malaysia by Huger (1966) and named it
as rhabdion virus of O. rhinoceros. In India, OrNV infected grubs after developing the symptoms could be
stored in the deep freezer at -40oC indefinitely retaining its virulence. Studies conducted at ICAR - CPCRI
indicated that OrNV infected grubs become less active and stops active feeding. As a result of virus
multiplication in the mid gut epithelium, fat body disintegrates and haemolymph content increases. This causes
translucency in the abdominal region which is an important exopathological symptom of the OrNV infection
and mortality in grubs. The infected beetles disseminate the virus through faecal matter into the surroundings
after 3-9 days of inoculation at the rate of 0.3 mg virus adult-1 day1. Introduction of OrNV in Minicoy and
Androth Islands of Lakshadweep, Chittilappilly, Thrissur, Kerala and Sipighat, Andaman Island successfully
reduced the population of O. rhinoceros and its damage potential on coconut.
Bacteria
A small number of entomopathogenic bacteria have been commercially developed for control of insect pests.
These include several Bacillus thuringiensis sub-species, Lysinibacillus (Bacillus) sphaericus, Paenibacillus
spp. and Serratia entomophila. B. thuringiensis sub-species kurstaki is the most widely used for control of pest
insects of crops and forests, and B. thuringiensis sub-species israelensis and L. sphaericus are the primary
pathogens used for control of medically important pests including dipteran vectors. These pathogens combine
the advantages of chemical pesticides and are fast acting, easy to produce at a relatively low cost, easy to
formulate, have a long shelf life and allow delivery using conventional application equipment and systemics (i.e.
in transgenic plants).
Mode of action
B. thuringiensis (Bt) is an aerobic or anaerobic facultative and sporulating bacterium (Figure 4). It can be found
in soil, insects and their habitats, stored products, plants, forest, and aquatic environments. It produces a
parasporal inclusion body (crystal) of protein origin, formed during sporulation and this crystal is composed of
Cry proteins which are encoded by Cry genes. After ingestion, the crystals are solubilized in the alkaline (pH 9
to 12) midgut environment. Some toxins are activated under alkaline conditions (CryII1A) and others are
activated under conditions of neutral to acid pH (Cry1b). Cleavage of Cry toxins is a crucial step in the
activation of the toxin and also in its specificity in different insects.
When toxins are solubilized, protoxins are released through the action of proteases resulting in active proteins of
6070kDa. The protoxins are activated by digestive enzymes in the midgut and bind to specific receptors in the
microvilli of the apical membranes of the columnar cells of the lepidopteran gut. The binding of Cry toxins to
the apical microvillus of the membrane vesicles of the insect determines the specificity of the Cry toxins. The
Cry toxins cross the peritrophic membrane by binding to specific receptors on the apical membranes of
intestinal cells causing opening or pore formation followed by vacuolation of the cytoplasm by osmotic
imbalance between the intracellular and extracellular environments and cell disruption. This destroys the
microvilli, causing the insect to stop feeding, leading to its death.
Success
Unlike broad spectrum chemical pesticides, Bt toxins are selective and negative environmental impact is very
limited. Of the several commercially produced microbial control agents, Bt has more than 50% of market share.
Extensive research, particularly on the molecular mode of action of Bt toxins, has been conducted over the past
two decades. The Bt genes used in insect-resistant transgenic crops belong to the Cry and vegetative insecticidal
protein families of toxins. Bt has been highly efficacious in pest management of corn and cotton, drastically
reducing the amount of broad-spectrum chemical insecticides used while being safe for consumers and non-
target organisms. Despite successes, the adoption of Bt crops has not been without controversy. In addition to
discovery of more efficacious isolates and toxins, an increase in the use of Bt products and transgenes will rely
on innovations in formulation, better delivery systems and ultimately, wider public acceptance of transgenic
plants expressing insect-specific Bt toxins.
Fungi
Entomopathogenic fungi do not require per os infection and could enter insect system through the cuticle.
Examples include Metarhizium anisopliae, Verticillium lecanii, Beauveria bassiana, Nomuraea rileyietcwell
exploited in pest management. Metarhizium anisopliae (Metchinkoff) Sorokin is an entomopathogenic fungus
which kills O. rhinoceros in conditions of low temperature and high humidity. The fungus could be mass
multiplied using cheaper substrates in both solid and liquid media and the spores could be harvested and treated
in the breeding site at 5 x 1011 spores m-3. In vermicomposting sites, treatments with M. anisopliae spores killed
all third - instar larvae, with the highest dose giving the fastest kill, taking eight days when favoured by high
humidity (Figure 5.a and b). This technology through farmer - participatory and women group approach has
created a great impact on the long-term bio-suppression of the pest in farmer-participatory and community-
mode. Mass production technology of M. anisopliae was standardized in semi - cooked rice grains yielding a
spore count of 3x107cfu / g of the culture.
Searching for natural enemies of coconut eriophyid mite A. guerreronis, ICAR-CPCRI could collect more than
40 isolates of the acaropathogenic fungus, Hirsutella thompsonii (Figure 5c). Based on the bio-efficacy studies,
one virulent isolate collected from Kayamkulam was characterized through molecular tools confirming species
identity. Coconut water was found as an ideal medium for mass production of H. thompsonii. Talc-preparation
of this H. thompsonii at 20 g L-1 of water palm-1 containing 1.6 x 108cfu with a frequency of three spraying per
year resulted in 63-81 per cent reduction in mite incidence. It was found effective in many locations, though
seasonal variation in efficacy existed.
Entomopathogenic nematodes (EPN)
The word ‘nematode’ means "thread-like” and they are also known as thread worms or round worms.
Nematodes are numerically the most abundant metazoans on earth and second only to insects, in terms of
diversity of forms (species) is concerned. Nematodes dwell in all types of habitats on the earth. Most of the
nematodes are free living which feeds on microorganisms. Nematodes also parasitize plants, animals and human
beings. There is hardly any animal on earth which is free from one or the other kind of nematode infection.
Entomopathogenic nematodes (EPN) of the families Steinernematidae and Heterorhabditidae are soil inhabiting
insect pathogens that possess potential as biological control agents. These nematodes, working with their
symbiotic bacteria (Xenorhabdus for steinernematids and Photorhabdus for heterorhabditids), kill insects within
24 to 48 hour (Figure 6). They are safe for the plant health, human health, soil and the environment. There is a
huge potential for the utilization of these nematodes for the management of many coconut pests like white grub,
rhinoceros beetle, red palm weevil etc.
Protozoa and Microsporidia
Protozoans are one-celled forms. One group the Microsporadia, contains many species that have promise for
biological control. Microsporidian infections in insects are thought to be common and responsible for naturally
occurring low to moderate insect mortality. But these are relatively slow acting organisms, taking days or weeks
to debilitate their host. Infected insects may be sluggish and smaller than normal, sometimes with reduced
feeding and reproduction, and molting problems. Death may follow if the level of infection is high. Nosema
locustae is the only commercially available species of microsporidium, marketed under several labels for the
control of grasshoppers and crickets. It is applied with insect-attractant bait. Because of its slow mode of action,
this product is better suited to long-term management of locusts than to the more intensive demands of
commercial crop or even home garden production.
Bio-scavenging
When plants and animals die, the organic matter that makes their bodies possesses energy in the form of
chemical bond. That energy is released by sequential breakdown of body tissue constituents. Insects, in feeding
on dead plant and animal tissues, often carry out the first stage in the decomposition process by pre-disposing
matter for enhanced decay and ultimate break down by microorganisms. Some prominent examples of insect
decomposers include termites that break down wood, spring tails that assist in the decomposition of dead leaves,
carrion beetles and fly maggots that feed on dead animals aiding scavenging and enhanced disintegration.
Rugose spiraling whitefly
Emergence of the exotic rugose spiraling whitefly (RSW), Aleurodicus rugioperculatus (Figure 7a) on coconut
palm during 2016 from Pollachi, Tamil Nadu and Palakkad, Kerala was the latest new addition of invasive pest
introduced into our country ably aided by inadequate quarantine approach. The pest could have been
introduced from Florida, USA either through ornamental palms or RSW-infested coconut seedlings. Being non-
native, RSW sounded alarm initially due to extensive feeding potential and high population build-up of the bug
on coconut palms. RSW feeds from undersurface of palm leaflet and the enormous honey dew excreted get
deposited on the upper surface of palm attracting the sooty mould, Leptoxyphium sp. Growth of sooty mould
Figure 6. (a) Larvae killed by Steinernematid nematodes
(b) Infective juveniles of EPN
(b)
(a)
affects the photosynthetic efficiency of palms and served as a characteristic feature of pest identification (Figure
7c).
Farmers are worried due to black encrustation of sooty mould on palms and other under story intercrops in the
system. RSW bred fast reaching as high as 15 egg spirals on a leaflet and with the white flocculent masses and
sooty mould development could panic any farmer in the initial phase. Gradient outbreak of RSW could be
realized interlinked with higher maximum temperature with lower humidity and rainfall as well. However, in a
period of four to five months, there has been tremendous build-up of the aphelinid parasitoid, Encarsia
guadeloupae (Figure 7b) which could bio-suppress RSW quite efficiently and significantly. From a modest 10%
parasitism initially registered, natural parasitism rose as high as 82% in a period of four-five months. This is one
of the classical success stories of conservatory biological control well documented and by this observation,
ICAR-CPCRI has recommended pesticide holiday to effectively conserve the natural enemy involved in RSW
suppression. Though
not well received, this strategy was well appreciated by the ecological benefit realized to nature as well as to
human health. The Organic Policy of the Government of Kerala is another boost in this direction that may also
encourage biodiversity preservation.
Sooty mould scavenger beetle
For the first time at the international level, scientists from ICAR-Central Plantation Crops Research Institute,
and ICAR-National Research Centre on Banana, Trichy have reported the occurrence of a sooty mould
scavenging beetle, Leiochrinus nilgirianus Kaszab (Coleoptera: Tenebrionidae) on coconut palms infested by
the rugose spiraling whitefly (RSW) (Josephrajkumar et al., 2018). This beetle, which resembles the predatory
lady beetle in appearance, are found to feed on the sooty mould deposits developed on the honey dew excreted
by the rugose spiraling whitefly (Figure 8). L. nilgirianus could be first located from sooty mould laden coconut
palms at ICAR-CPCRI, Regional Station, Kayamkulam during July-August period which coincided with the
south-west monsoon phase providing high humidity and morning wetness, that favoured the accurate niche for
enhanced survival and feeding.
All stages of the beetles viz., eggs, grubs, pupae and adult beetles were found on the palm leaflets and other
intercrops with sooty mould. Generally, the grubs and adult L. nilgirianus beetles are restricted on the under
surface of the leaves. But they move on to the upper surface of the leaves with sooty mould deposits during
early morning hours with dew drops and feed on the sooty mould. Eggs of this beetleare purplish, laid in
groups and emerging neonates are transparent and turn black, assume spherical and cylindrical shapes in
movement due to the presence of elastic inter-segmental membrane. Creamish patches are developed during pre-
pupating stages and pupae with distinct cream patches are also confined on the under surface of palm leaflet
indicating its photo-
sensitiveness. During our observations, more than five beetles (Average 2.07±0.9) and immature grubs could be
noticed on sooty mould laden leaves. Bristle-like tarsomeres and tarsal claws of adult beetles encouraged
effective adhesion, scooping of mould and swift movement on fungal growth. L. nilgirianus population was
found very high and subsequently got reduced with the decline in RSW population and the sooty mould
deposits. Mouth parts and gut lining of the beetle with fungal deposits could be located confirming the
scavenging action of the beetle. Though ecosystem services provided by insects include food for wildlife, pest
destruction, crop pollination, scavenging, etc.which is estimated at around $57 billion in the United States of
America alone, a thorough cleaning action on an economically significant crop like coconut is reported for the
first time at global level. Habitat conservation of the sooty mould feeding scavenger beetle, L. nilgirianusin
the palm ecosystem is very crucial and the conducive weather factors of high humidity and high rainfall
prevailing in Kerala during monsoon phase are key factors for the survival and feeding efficiency of the beetle.
Though report on scavenging action by insects such as termites disintegrating wood, springtail decomposing
dead larvae and fly maggots feeding on dead animals exist in nature, the present instance appears to be unique in
which sooty mould deposition is totally cleared by an insect scavenger on palms. Conservation of E.
guadeloupae by limited or zero pesticide usage coupled with in situ habitat preservation of scavenger beetles (L.
nilgirianus) appears to be a very effective strategy that would help in controlling A. rugioperculatus and in
clearing sooty mould from coconut palms at no cost in the most natural and eco-friendly manner avoiding
chemical management options and other expensive methods. Furthermore, the Organic Policy adopted by
the State Government of Kerala could have encouraged the sustenance of the beetle and emerged in need for
scavenging action.
Ecological Engineering
Ecological engineering defined first by Odum (1962) is a human activity that modifies the environment
according to ecological principles. Accordingly, it is a useful conceptual framework for considering the practice
of habitat manipulation for arthropod pest management. Habitat manipulation aims to provide the natural
enemies of pests with resources such as nectar, pollen, physical refugia, alternative prey, alternative hosts etc.
The development of ecological engineering ranged from a simple first approximation that diversity is beneficial,
to contemporary understanding that diversity can have adverse effects on pest management. In the recent era of
agricultural intensification, the potential for using crop diversity to manage insect and microbial pests has not
been extensively exploited.
Push-pull strategy
Push-pull strategies use a combination of behavior-modifying stimuli to manipulate the distribution and
abundance of pest and/or beneficial insects for pest management. Strategies targeted against pests try to reduce
their abundance on the protected resource, for example, a crop or farm animal. The pests are repelled or
deterred away from this resource (push) by using stimuli that mask host apparency or are repellent or deterrent.
The pests are simultaneously attracted (pull), using highly apparent and attractive stimuli, to other areas such as
traps or trap crops where they are concentrated, facilitating their elimination. The strategy is a useful tool for
integrated pest management programs reducing pesticide input.
An agro-ecosystem based pest regression strategy by including compatible intercrops in coconut-based cropping
system has registered lower pest incidence (Figure 9). The influence of mixed-volatile cues of crop plurality
(rambutan, nut meg, curry leaf, banana, turmeric, red gram, papaya) inflicted lesser rhinoceros beetle damage
(15.8%) compared to palms in outer whorls (30%). In situ stimulo-deterrent diversionary strategy infused less
pest damage and encouraged more defender population through eco-feast crops (Antigonon leptopus) and
diversity in fruit crops. In addition to pest regression, continuous employment and income is generated fostering
closer care to palms complementing the concept of an “inch of land and a bunch of crops”.
Plant health management
Plant health management (PHM) is the science and practice of understanding and overcoming the
succession of biotic and abiotic factors that limit plants from achieving their full genetic potential as crops,
ornamentals, timber trees, or other uses. Although practiced as long as agriculture itself, as a science-based
concept, PHM is even younger than integrated pest management (IPM) and includes and builds upon IPM; but
is not a replacement for IPM. PHM is a moving target, like a football game, where one team is science and
technology and the other is nature, where the S & T team is only beginning to know nature's rules while playing
itself with the three sets of rules written to, respectively, satisfy the laws of economics, protect the environment,
and gain social acceptance. In a nutshell, PHM includes integrated pest, disease and weed management,
integrated nutrient management and soil health management in a holistic manner as system approach.
From the ecological engineering concept, health management is revered as holistic and at the same time
sustainable providing continuous income and employment as well. Systematic care would thus make you cheer
with coconut and empower your health infusing bio-happiness.
Financial support and sponsorship
Nil
Conflict of interest
There are no conflicts of interest.
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