|Integrated pest management:
Looking back and forward
Since the 1950s, there
has been unprecedented concern over the environmental
and public health problems associated with the
use of chemical pesticides on the basis of
the message carried in the book Silent
Spring that deals with a new pest management
strategy that integrates disciplines like agronomy,
genetics, biology, and chemistry. Thus, this strategy
forms the Integrated Pest Management (IPM). Efforts
to implement IPM revealed poor adoption in
case of resource poor farmers, though effective for
industrial farming areas. Yet, the preferred approach
for the present and future is IPM. Farmers
desire that IPM strategy should be simple,
easy to operate with sizeable economic returns.
Thus, much depends on developing a perspective
of stewardship rather than domination over nature.
If tradition is made the foundation for modernity
coupled with use of such chemical levels that
enhance overall efficiency, its acceptance by farmers
is assured. That would ensure ecological viability
and economic sustainability to crop production endeavours.
Over the past years, high academic,
industrial, and financial support have been extended to plant protection in general, and
integrated pest management (IPM) in particular. The annual estimated losses through pests
and pathogens of crops (pre- and post-harvest), soil nutrients robbed by weeds, and ill
health of animals run into several billion dollars in value. However, both the chemical
and non-chemical measures have failed. Further, IPM strategy which used chemical
pesticides as the last resort has a long recorded history; with divisive debates and
discussions on it. All reports, publications and media coverage either whole-heartedly
promoted an environmental agenda or rejected such an agenda outright. This review on the
subject outlines historical perspectives, examines the strengths and weaknesses of its
various components, provides current academic strategies that suggest the policy frame for
research extension and adoption in the field, and illuminates the hazy and controversial
areas to reconcile the two major concepts: chemical warfare to eradicate the
pest a flagrant act; and management to control the pest as a sovereign
Historical developments in pest control and management
Ascent of chemicals and pesticides
The forerunners of todays chemical pesticides
appeared early on in history. The Sumerians used sulphur to control insects and mites
around 2000 BC. Biblical writings frequently refer to the plagues caused by locusts;
remains of grain-eating beetles were found in vases in king Tutankhamens tomb dating
back to 1350 BC. With the birth of Christianity, rituals were developed to control
pests that caused havoc. Romans added many formulations with olive oil and sulphur for
controlling pests. Pest management by the Chinese showed high degree of sophistication
growing out of their long experience with rearing silkworm moths. Historical records exist
that show the use of herbs, oils and ash to protect seeds and stored grains, as well as
biological methods to control growth of caterpillars and beetles in citrus orchards, using
predatory ants. A large part of renewed interest in pest control grew as a result of
dramatic growth in agriculture and improved crop production with improved irrigation
methods and use of fertilizers. The discovery of organic
pesticides chemi-cals that could be easily
manufactured proved to be of great success and won the appreciation of
The four groups of organic insecticides
(organo-chlorines, organo-phosphates, carbamates, and pyrethroids) are in use in our win
over nature, of which DDT is the flagship chemical, and which fetches for its discoverer,
Paul Muellers, the Nobel prize1. In a decades time, a gigantic industry
for the manufacture of various insecticides was established in the industrially-developed
countries, which subsequently expanded its base in the developing countries as well.
Major policy shift: Descent of chemicals
Globally, agriculture has switched to the use of
machinery as labour saving, earliest practised in US. In both India and Japan, land is a
limitation which has been compensated by the HYV technology, based on use of fertilizer
and modern irrigation practices to increase the yield. The use of pesticides in the
post-war industrial agriculture of US, and the green revolution in India witnessed three
periods. (i) Euphoria and the crisis of residue (194555). (ii) Confusion and the
crisis of environment (195572). (iii) Changing paradigms (1968 to date). In
the first period the success of industrial agriculture was hailed, and the use of
pesticide, which gave boost to the pesticide chemical industry, made termination of some
insect pests a reality. However, this was followed by a period of confusion and doubt due
to the two warring groups for and against the use of pesticides. The book by Carson1
virtually gave a death blow to the indiscriminate use of chemicals to control pests.
Further clinching evidence in support of Carson came from the ban imposed on the use of
DDT for crop protection. The final period changing paradigms
marks the beginnings of ecologically friendly policies and the serious search for
alternatives, giving birth to IPM where chemicals are to be used only as a last resort.
The book by Carson essentially brought two issues
into sharp focus: (i) Chemical pesticides can be dangerous to human beings as well as the
environment and should be used as the last resort. (ii) There are biologically-based
alternatives to synthetic pesticides, and these ecologically friendly methods need to be
studied and implemented. The message though reasonable in the light of our current
problems, but when first appeared whipped up reactions; often from people who had not read
it and by the people who had vested interests in chemical industry. But, devastation
wrought by indiscriminate use of pesticides, for example DDT, has brought home the message
of Carson, and recent policy makers are in tune with her message. Thus, the policy adopted
by World Bank since 1982 is to finance projects that do not seriously compromise public
health or cause irreversible environmental deterioration. However, the World Bank
objective should be to focus on the IPM approach for sustainable agriculture.
Some of the experiences of US agriculture have
further weakened the popularity and wider acceptance of chemical control of insect pests
and pathogens: (i) Over the period 194274 losses from pathogens increased from 10.5
to 12% and those due to insects doubled from 7.1% to about 13% despite a ten-fold increase
of insecticide application2. (ii) Losses from weeds declined over the same
period in USA largely because of improved technology of mechanical cultivation in addition
to the use of herbicides3. The former has been attributed to: increasing
resistance of pathogens and insects to pesticides; the destruction of natural enemies of
certain pests; and reduced practices of crop rotations and crop diversity with greater
reliance on continuous culture of mono crops. In the tropics as well, these factors are
operative to which must be added the problem of resurgence of pests following repeated
insecticide applications. Since the 1950s, such resurgence has been documented for green
rice leaf hopper and plant hopper after the use of broad-spectrum insecticides, such as
DDT and BHC, to control such major pests of rice in Asia as the rice borers4.
Thus, whereas chemical control is philosophically
based on a sense of nature dominated by human technology, the term management emphasizes
the comprehensive nature of the approach together with the ecological realities5.
Integrated pest management
The term pest management was first used by Bartlet6,
and later on elaborated by Stern7, as a concept of integrating the use of
biological and other methods of controlling pests. This was later broadened to include the
coordinated use of all biological, cultural, and artificial practices. Subsequently,
various authors advocated the principle of incorporating the full array of pest management
practices together with increased-production objectives, thereby making it into a total
system approach8. Since IPM deals with pesticide management and not pest
management, it cannot be denied that its major thrust is for reduction of insecticide use.
This approach needs to be further researched to understand the complex interaction between
ecology, agronomy, biology, and climatology to develop it into an ecologically-based
disease and insect control strategy, which represents only a part of an overall
In integrated pest control (IPC), pesticide is used
only when the size of pest population warrants less damage to the natural enemy complex
and the environment, with ultimate economic benefit accruing to the farmer. Currently,
this covers any combination of different control technologies, although it is central to
the concept of wiser use of pesticides. The combination of these two strands, IPC and pest
management, have resulted in the IPM. Moreover, IPM is the philosophical
precursor for another popular philosophy: sustainable agriculture9.
The present IPM thesis is a composite of disease management and integrated crop management
The total system approach
Essentially the IPM paradigm is: (i) Eradication not
as the goal, but only application of minimal level of control that will maintain the pest
below the economic damage threshold. (ii) It accepts multiple techniques in preference to
following only one pest management strategy. (iii) The no-option goal in reducing the
levels of pesticide use, and least or no damage to the non-target organisms and
ecosystems. (iv) The need for indigenous knowledge of agricultural systems and pest life
cycles to complement basic science and technology10. IPM may thus be an
excellent fit for industrial agriculture, but its transfer to resource-poor farmers in
developing countries is problematic. Technological change is not socially or culturally
neutral11. The transfer of strategies of developed countries where IPM
succeeded to developing countries showing different ecological cropping patterns and
cultural practices, is naive. Furthermore, IPM programme so far operated only to limit
pest populations. Thus, a pesticide management programme objective which relegates the
pest management objective which is equated to treat the symptoms approach
would be a major strength of real IPM. Also, though deemed as more complex to academic and
extension officers and farmers, there is the need for more simple and straightforward
solution to determine the economic threshold for each crop location set up. The terms pest
control or pest management or crop management prefixed as Integrated, endorse
a need for a total system approach wherein there is a meeting of minds, materials, and
Adoption of IPM by poor
IPM originated in the high-input agricultural
systems of developed countries, particularly North America. For developing countries, the
regular use of pesticides is limited to the relatively small areas of high-value
commercial crops and vegetable gardens in the urban environs. The major obstacle for the
widespread adoption of IPM in developing countries has been brought into focus by Gooch12,
Corbet13, Morse and William14, World Resource Institution15,16,
and Huis and Meerman17. The major findings of these studies are: (i) The
limited economic returns accruing in traditional farming systems rarely carry economic
justification for pesticide use. Nearly all the cultural practices under cropping systems
with many varieties confer enough control over pests to be within economic threshold of
pest damage. (ii) Crops grown in developing countries, largely on small holdings, by
resource-poor farmers meet local need and nearly none for export. But in developed
countries, commercial crops of great value for export, like cotton, and the increased
demand for livestock, aim for maximum yields and not economic maximization.
Agronomic and cultural: There
exist a number of physical and mechanical methods of pest control which are non-chemical
in nature and farmers traditionally have more confidence in these methods. Some of these
could be modified, thereby leading to more effective and economical methods of pest
control. For example: (i) Storage of food grains suffer from an array of pests, resulting
in significant loss both in quantity and quality. Such damages can be reduced through use
of low-energy radiation, thereby reducing moisture content in grains to safer levels. The
electrical properties of the pests are sufficiently different from the matrix such that
the pest tissue is heated more than the grain and this either repels or kills the pest
without a fire hazard. The development of affalotoxins in the storage of peanut is
(ii) Some serious diseases, like the red rot of sugarcane, are prevented when the
sugarcane setts (seed material) are allowed to remain in boiling water for a short while
and then used for planting. (iii) Traditional practice of preserving many of the vegetable
seeds is to set the seed in dry dung cakes which are subsequently preserved in mud pots,
along with dried neem leaves. The seeds retain their viability and vigour when sown. (iv)
A more widely practised method of soil sterilization to eliminate the pests and crop
diseases is achieved through burning crop residues, sugarcane trash, rice stubble and
straw: a process known as rabbing. Many of such traditional practices of
merit, are slowly losing ground.
Although cultural methods do not usually offer a
high level of pest control, these typically involve minimal extra labour and costs. More
recently, one strand of IPM approach is to revive cultural methods of control. A healthy
plant exhibits high degree of tolerance to pests and diseases. The converse is also true.
Therefore, some practices like right time of sowing, harvest, deep ploughing, etc. do help
pest control by its avoidance. Furthermore, crop sanitation, i.e. removal of sources
(foci) of diseases, such as diseased and damaged plants, leads to reduction of pest
Experimental results on irrigated rice in
Philippines showed that use of chemical sprays, wherein nine sprays are used per season,
gave a net benefit of 11,846 pesos/ha (excluding health costs), while natural
control, adopting only more integrated and sustainable practices, registered a net benefit
of 14,009 pesos/ha18.
Biological: Biological control encompasses a
wide spectrum of use of biological organisms and biologically- based products including
pheromones, resistant plant varieties, and autocidal techniques such as sterile insects.
It also includes such cultural practices as crop rotations, mixed and multiple cropping
with varying plant densities, and genetic heterogeneity.
Paul DeBach19, an authority on
biological control, estimated that using natural predators led to at least 120 species of
insect pests under some degree of control. Most successful cases of its use in India are
in: (i) control of sugarcane stem borer pest with the related parasite Trichograma
sp.; (ii) control of prickly pear with cochneal insect Dactylopus sp.
Use of biological control resulted in saving the
staple food crop cassava in Africa, grown over 200 mil acres, and benefited the
farmers to an estimated value of $ 3 billion. This project used massive aerial
spraying of the parasite, a tiny wasp, on the mealy bug20. Biological control
of weeds has also been widely reported in: the use of spore suspension of a fungi Phytophthora
palmivora for control of weeds in citrus in US, and a dry powder formulation of Colletotrichum
gloeosporioides for the control of weeds in rice and soybean21.
Thus multiplication and release of known natural
enemies in standing crops has succeeded well since first tried in the 30s. It is
still in practice, though strongly eclipsed by the synthetic pesticides.
This is an ecologically sound approach to pest
suppression because, once established, it is quite permanent, non-disruptive, and often
The promotion of bio-pesticides (e.g. Trichoderma,
Trichogramma, Helicoverpa NPV, Spodoptera NPV), which are similar to what the natural
enemies or the host plants produce in their defense, hold promise for the future. These
have largely reduced the use of chemical pesticides.
Chemical control as the last resort in the IPM
philosophy could be availed with enhanced and accurate knowledge of pest behaviour and
insect population cycles. This would enable scientists and farmers to pin-point and
restrict chemicals to the time and place where it is most effective against the pest and
least harmful to the environment including human health. Moreover, the resistant varieties
of crops need vigilant monitoring. Pest outbreaks sporadically may adopt to a widely
planted resistant cultivar before the resistant factor has ever been useful in reducing
economic losses due to pest22.
The use of pheromones now widely used on cotton
commercially worldwide for mating disruption, resulted in control of pink boll worm in
Egypt, Pakistan, Turkey, and Greece where these have been successfully deployed as
stand-alone control products. In India, development work is well under way for the control
of rice stem borer Scirpophaga spp. by mating disruption, following its very
successful deployment against the striped stem borer (Chilo suppressalis) in
A diverse group of natural molecules that may also
be regarded as potential herbicides termed as allelo-chemicals are now known.
These compounds are released by a plant into its immediate environment to retard or
prevent the growth of other plants so as to achieve competitive advantage in a given
environment. Chemicals with such allelopathic potential are present in virtually all
plants and may be released by the volatilization of root exudates, leaching or
decomposition of plant
Semio-chemicals: Modern pest management
switched over to the use of naturally occurring chemicals, some made by insects themselves
and used to control their behaviour. These are the semio-chemicals: the broad term for
insect attractants and other behaviour-modifying chemicals widely adopted as key
components of IPM. These are the pheromones (sex attractants and aggregation agents). The
development of active pheromones for most major pests and their formulation in lures for
deployment in custom-designed insect pest traps, is increasingly providing information
required to complement and sustain rational insect/pest management systems. Thus,
monitoring traps offer four benefits: (i) early detection and location of infestation,
(ii) an indication of the severity of infestation, (iii) determination of the most
favourable time for control measures to be applied, and (iv) a quality control aid.
Pheromones claim several advantages such as: (i) highly active at low concentrations, (ii)
total volume for the world needs is a few pounds per year, (iii) though their synthesis is
complex and costly, it needs only a well-equipped lab and not an industrial unit for their
production, and (iv) no side effects and no residue problems. All that it needs is
monitoring, attract, kill, and mating disruption. Research on semio-chemicals can provide
an alternative to outsmart pests without synthetic pesticides. Pheromones as an industry
have not yet developed. Total 1991 sales were only $ 38 million from 17 North
American firms that synthesized 139 different products.
The two significant products, boll weevil and pink
boll worm pheromones, must face two barriers: (i) natural extracts from female codling
moth glands were 1200 times more powerful and effective in attracting male moths than an
equivalent amount of synthetic product, (ii) the product being sensitive to light
decomposes into inactive compounds and therefore should be used only after sunset and
(iii) low doses will not be enough and higher doses would combine waste and cost.
However, semio-chemicals have not proven to be a
commercially attractive alternative to pesticides. The reasons are many and complex, but
the bottom line is: pesticides are cheaper to buy and apply than pheromones; are easier to
use; and are more consistently effective25.
Genetic engineering: Pest resistance
represents the ability of a specific crop variety to produce a larger crop of acceptable
quality compared to ordinary varieties, given the same level of insect (pathogen)
population. The inheritance of resistance to specific pest is controlled by a single gene,
monogenic (specific) or more than one, polygenic. It is difficult to determine how long a
newly developed resistant variety will remain resistant. Hence constant vigilance on
resistance functioning is recommended. Four types of resistance recognized are: avoidance,
non-preference, antibiosis, and tolerance. For cultivated crops grown on large-scale by a
single variety, like IR-8 rice in India, both vertical and horizontal resistance become
Some 10 to 15 generations of insect pests are
required for the manifestation of resistance. Currently, more than 500 species of insects
show resistance to one or more chemicals and few serious pests resist nearly all the
poisonous pesticide chemicals. Indigenous people in their traditional methods in the
centers of evolution of specific crop are well aware of varietal resistance to pests. It
is on record that South American Indians grow cassava as their staple food, and in Brazil
22 varieties are recognized, 50 in Peru, and 140 in Rio Negro.
The promise of engineered resistance is through
breeding crops for pest resistance. Such resistance should preferably be horizontal than
vertical. CIMMYTs Tuxpeno group of maize lines has been notable for disease
resistance. The incorporation of resistance to streak virus in some new maize materials by
the International Institute for Tropical Agriculture (IITA) has deservedly been
recognized. Such technologies add the dimension of resource neutrality in technology
development. The solution to pests showing resistance may lie in using bio-engineered
plants that do not overkill the pests. Thus, resistance management in transgenic plants
might include production of lower doses of toxin, multiple toxins, and sporadic rather
than continual toxin release. Further, escape from toxins could be provided in transgenic
crop by designing crops that turn off toxin release at a certain point in plant
development or release toxin only in specific tissues rather than entire plant.
Bio-engineered crop plants: In
terms of integrated management of pests, the most important breakthrough has been the use
of genetically engineered crops to confer resistance via the inclusion of genes expressing
Bt toxins, cowpea trypsin inhibitor or secondary plant metabolites26.
Transgenic crops with enhanced resistance may be used within the IPM programmes27.
Bacillus thuringiensis (Bt) products are the most frequently used for
natural biological control. But Bt spray is active for a short period and very expensive
too. A better way to circumvent this problem is to insert bacterial genes producing the
toxins directly into the plants on which the insects feed. A number of crop varieties such
as corn, cotton, potato, and tomato are commercialized wherein each transgenic crop
contains genes effective against an important pest of that crop. The pest insects feeding
on these transgenic crop plants are quickly poisoned and thus there is no need to spray
the fields with insecticides. But Bt genes as such may not express as efficiently as plant
At present, 28 varieties of genetically engineered
plants expressing several agronomic traits have been allowed to go for commercialization
in the United States. Some of these are commercialized in South America, Japan and
Australia. Economics-wise, a potato farmer in US spends $ 359 per acre for chemicals
against Colorado potato beetle, while Bt seeds cost only $ 22.5.
Concerns over introducing transgenic plants focus
on four major areas: (i) human health risks associated with food contamination, (ii)
potential for the transplanted genes to jump across crop plants to weeds, (iii) increased
herbicide use that would result from planting herbicide-resistant crops, and (iv) pest
resistance to transgenic organisms. The control of gypsy moth pest on fruit trees with Bt
sprays was successful, but the size of success was uncertain. Yet, it is preferable to
chemicals. B. thuringiensis is a common spore-forming bacterium that is
non-pathogenic to warm-blooded animals but is highly pathogenic and specific to larval
butterflies and moths. The effectiveness of Bt is due to the protein secreted by the
bacterium, that kills the moth.
There appears to be little risk to trying most
bio-engineered plants with considerable potential to reduce the use of chemical
pesticides. The gene products produced by transgenic plants do not suggest toxicity to
people or animals. The transgenic plants in super markets need no labelling as they are
deemed identical to conventional varieties as food products in all respects. One problem
with transgenic plants is that negative ecological consequences would result from some
traits being incorporated into crops, especially herbicide-tolerance. The concern here is
that an herbicide-tolerant domesticated crop/plant could revert to a wild weedy state to
become a pest25.
A recent workshop at M.S. Swaminathan Research Foundation, Chennai related to bio-safety
issues concerning transgenic plants, recommended that each country should develop a set of
safety guidelines which should be flexible to accommodate case to case variations and
emerging technical developments29.
Herbicide use for weed control: Crop
plants suffer severe competition from weeds for three important inputs: solar energy,
water, and nutrients. About 250 species, or 0.1% of the worlds flora, are known to
be sufficiently troublesome as weeds in crops. Of these, 70% are found in 12 families, 40%
alone being members of Graminae, and Compositae. Interestingly, 12 crops of five families
provide 75% of world food, and the same five families provide many of the worst weeds.
Weeds act as reservoirs of disease organisms and as alternative hosts for insect pest.
Some major crop pests actually prefer to lay their eggs on weeds rather than on crop
plants. Some of the known reasons for persistence of weeds are due to C4 photosynthesis,
high seed production per plant, seed maturity coinciding with the harvest of the crop
plant, resistance or tolerance to herbicides, ability to overcome mechanical control by
vegetative regeneration, and discontinuous germination over prolonged periods30.
Biological control of weeds are on record. Thus use of spore suspension of fungi Phytophthora
palmivora for control of weeds in citrus in US and a dry powder formulation of Colletotrichum
gloeosporioides Sacc. for weeds in rice and soybean, are illustrative21.
A diverse group of natural molecules that may also
be regarded as potential herbicides, are the allelo-chemicals. These chemicals are
released by plants into its immediate environment to retard or prevent the growth of other
plants so as to achieve a competitive advantage in a given environment. Chemicals with
such allelopathic potential are present in virtually all plants and may be released by
volatilization, root exudation, leaching or decomposition of plant residues.
Thus, weed control of tomorrow, will require the
farmers to work not against, but with the weeds.
Biotechnology: This is a generic term that
includes many techniques to provide a wave of new products for pest management. However,
the main hope for IPM is largely based on the use of genetic engineering techniques, or
more precisely the recombinant DNA technologies. It is ironical that IPM will benefit from
a technology that is largely under the same control of multinationals that produce
pesticides and that generate products having negative environmental impacts similar to
those of pesticides. However, this industry should focus on using genetic manipulation and
other techniques to increase the virulence and host range of biopesticides, instead of
designing them as mere complements to natural strengths. Biotechnology, relative to other
technologies, needs careful assessment. The possibilities of a more lasting progress in
ecologically sound pest manage-ment and sustainable agriculture will result from
agro-ecological research focused on redesigning the structure and operation of
agricultural ecosystems31. The results of recent survey in US on the relative
importance of various pest management technologies show its importance (Table 1). At
CIAT (Columbia) improvement of cassava production researches see the potential of
biotechnological tools to increase access to genetic diversity and efficiency of field
testing. On the basis of molecular marker technology, candidate gene loci for
resistance have been identified. At CIP (Peru) genetic maps of two important crops, potato
and cassava, and analysis of their quantitative resistance traits are in progress32.
We have on hand a landmark document of UNEP and
CIPE under the caption Beyond Silent Spring33, and an illuminating
literary achievement on the subject by Mark L. Winston25 which are of immense
guidance with a balanced approach for a pragmatic policy on this subject. Both the books
are woven on the same basic strands: mutually supportive of the polarized perceptions, and
The future of IPM
IPM embodies an ecological approach to the pest
problem with the sole objective of reducing or eliminating use of chemical pesticides. The
gains are reduction in costs of production, more economic access of food to the poor, and
conservation of the resilience and integrity of the ecosystem. On a reasonable
computation, a land saving of 40 to 50 mil.ha of land is a reality. The common way of
measuring pesticide chemicals use (as kg/acre) that widely differ in their active toxicity
ingredients may not be correct and may lead to such levels which are uneconomical and more
hazardous as well. The TU (toxicity units) and TPU (toxicity persistent unit) indexes are
simple measures related to potential for exposure to chemicals with health effects. The
need for extension agencies to guide the farmers is urgent and imminent34. All
available and recorded evidence, as of today, eloquently endorses that pests can at best
be controlled or managed, but not eradicated.
If the green revolution is to be sustainable, a
modified IPM based on ecological principles close to nature is the only alternative.
Looking back, is to capture the traditional wisdom of our agriculture, while looking
forward is to avail relevant modern advances of science, of which IPM is an essential
component. With the former as the foundation and the latter as the superstructure,
sustainable food security system can be built: the need of the next millennium.
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Received 4 June 1998; revised accepted 2 July 1998
|Behavioural dynamics in the
biological control of insects: Role of infochemicals
T. N. Ananthakrishnan
Infochemicals tend to serve
as messengers mediating interactions among host plants,
insects and their natural enemies, parasites and
predators having exploited the release of plant-produced
chemicals as cues to locate their hosts and
prey. Volatiles from such host plant complexes
may emanate from the plant, the host insects
and host by-products such as faeces. Plants
therefore are vital sources of information for
natural enemies. In many cases kairomones emanating
from the herbivores act alongside the host
plant components and are successfully utilized by
the natural enemies in their host-finding process.
The behaviour and success of natural enemies
undergo considerable variation when the insects colonize
different host plants and modify the behavioural
sequence of natural enemies. Host habitat selection,
host selection and acceptance are modified by
a number of chemical stimuli resulting in
a continuum of behavioural exercises linking biological
control with the allelochemical web. Some of
these aspects are discussed with emphasis on
cotton boll worm natural enemy interactions.
the involvement of the host plant, insect and natural enemies in effective and sustainable
pest management strategies has revolutionized the concept of biological control of
phytophagous insects. Tritrophic interactions, as these are known, essentially focus on
the abilities of natural enemies to use plant traits to locate insects, besides
emphasizing on the ecological and evolutionary implications of the food chain1,2.
In long or short-range locations of their insect hosts natural enemies use the host plant
traits which influence their ability to detect and utilize insect hosts, so that
phytochemicals enhance attack by natural enemies. Insect damage-induced chemical and
physical responses of plants influence the biology of parasites so that a phytochemical
connection becomes established at different trophic levels. The release rates of
infochemicals tend to differ altering the quality of the host insects to the parasitoids.
Chemi-cal, tactile or visual cues enable the natural enemies to distinguish between
infested and non-infested plants. The question as to whether plants release chemicals to
attract parasites or whether parasites have evolved to detect these cues is a relevant
one, involving coevolutionary implications.
Plant odourants dominate the atmospheric chemical
environment forming aerial bouquets and insects including parasites select a
few critical signals that stimulate their behavioural patterns. Plants respond to insect
feeding by releasing volatiles that attract natural enemies which in turn attack insect
herbivores. Many parasitoids occur in specific habitats within which their hosts occur,
habitat location forming an important aspect in their host selection process. Plant
phenotypic variation plays a role in structure of parasitoid communities, often
determining their composition3. Numerous ecological and physiological factors
tend to influence this process of host location directed by signals originating from the
microhabitat, plant, host insect or microorganisms. In this exercise they respond and use
specific cues from host plants to locate them, including those from damaged plant leaves
and odours from host insect faeces47, so that natural enemies base their
foraging strategies on chemical information from the first and second trophic levels810.
While three trophic levels are common, the existence of a fourth is not uncommon involving
the host plant, insect, predator and its parasitoid, as in the case of the soyabean
looper, Pseudoplusia includens. Since antibiosis can have an effect on
organisms through four trophic levels, the specific relationship between organisms of
various trophic levels is important in determining host resistance. The predator Podisus
maculiventris is at the third trophic level with the parasite Telenomus podisi
at the fourth trophic level11.
Natural enemies have exploited plant volatiles to
locate their hosts and volatiles emitted by faeces of larvae may also be involved in
orientation. Larval faecal volatiles may be related to the breakdown process of plant
material after digestion by larvae. The presence of other volatiles may be the end product
of the process related to microorganisms inhabiting the faeces12.
Induced defenses as signals to natural enemies
Volatiles released by damaged plants after insect
feeding tend to increase the efficiency of natural enemies and plants producing such alarm
responses attract more parasitoids and predators13. Being detectable these
natural enemies learn to associate the volatiles with the prey. Induced defences increase
emission of plant volatiles greatly and being diverse in chemical composition, the nature
of their blends tends to be complex, changing with increasing induction. A whole suite of
chemicals are released by damaged Brassica oleracea such as isothiocyanates,
which are hydrolysis products of glucosinolates, undamaged plants emitting them in smaller
amounts as also several terpenoids14.
Intraspecific host plant variation that influences
parasitoid success has been evident in both agricultural and natural systems and varietal
differences in crop plants are known to influence parasitoid preference due to change in
the nature of volatiles so that the role of plant phenotypic variation becomes important
in the behavioural diversity of parasitoids. It is this intricate interaction between
plants and natural enemies such as parasitoids that acts as a driving force leading to the
production of adequate signals affecting the behaviour of natural enemies in a positive
way. The parasitoids make use of these volatiles to identify the vicinity of host-infested
plants, in particular the orientation of the larval parasitoids to the frass of host
larvae, since they are in a position to identify the damaged plants from a distance1517.
Foraging parasitoids like Microplitis croceipes would be exposed to a wide
range of volatile blends both from host plant and insect complexes in its environment.
Learning by parasitoids enables behavioural variability, recognizing the odour of hosts as
well as their exact site and environment. On the basis of information acquired immediately
upon emergence from host puparium and during the first oviposition, they learn more in
accordance with odours acquired by the host18.
Divergent views exist regarding the role of induced
defenses on herbivores, providing reliable signals to natural enemies indicating the
presence of host insects. The view that plant volatiles have evolved to serve tritrophic
communication is supported by evidence that release of green leaf volatiles increased
after insect herbivore attack with many parasitoids and predators being attracted to the
damaged host. Localized induction tends to increase the activity of phytophagous insects
within the plant19 enabling easy detection by natural enemies. Induction of
allelochemicals may prolong development of host insect larvae making them more susceptible
to the natural enemies or as in many cases allelochemicals may simultaneously reduce
growth and attract more natural enemies20. Indirect effects of induced
chemicals relate to their ability to prolong development of insect larvae, enhancing the
possibility of natural enemy attraction20. Constitutive variation in
phytochemistry as well as induced responses in plants after insect attack form the basis
for phytochemical involvement with the third trophic level21 25.
The behaviour and success of natural enemies undergo
considerable variation when insects colonize various plant species including crop systems
in response to different volatile compounds, modifying the behavioural sequence. With
regard to the specificity of an insect herbivore to a plant species and that of the
parasitoid to the insect, genetically evolved responses to insect hosts and plant odours
tend to aid in host-finding. Instances are known wherein innate responses are replaced by
associative learning26 as evident in the case of more generalized insect hosts
and parasitoids, where the use of specific kairomones and synomones play a role so that
the informational value of the stimuli depends on two factors insofar as parasitoids are
concerned, viz. their reliability indicating available and suitable hosts and
detectability of the stimulus with ease, both the factors tending to increase searching
efficiency27. Reliability of plant cues depend on the periodicity of plant
infestation over space and time and natural enemies combine the advantageous aspects of
information from both trophic levels. When a parasitoid population is generally associated
with a particular host species and its host plants, the parasitoid is expected to show
high innate responses to these cues which act as reliable indicators of host presence.
Host-derived stimuli are most reliable in indicating host presence, accessibility and
suitability28. Species-specific chemical cues that reliably identify plant
species are not always available to parasitoids, so that learning tends to become an
important aspect in enabling the parasites to find their hosts. Noldus et al.29
have shown that the sex pheromone of Mamestia brassicae females were
adsorbed on to the leaf surface of Brussel sprouts to such an extent that it was capable
of eliciting behavioural responses from Trichogramma evanescens. This
illustrates the involvement of host habitat cues to close range host acceptance cues. In
many instances kairomones emanating from the herbivores act alongside with host plant
components and are successfully utilized by the parasitoids in their host-finding process3032.
Therefore, a close understanding of the intricacies of behavioural diversity of
parasitoids appear essential in generating increased success in biological control
Natural enemies use substrate features of the host
plant, in long- and short-range location of their resources, prey or host33. At
short distances host-finding is readily accomplished, egg parasitoids being strongly
influen-ced by host kairomones. As long-range cues, chemical features are used by
parasites in locating their hosts3436. Pheromones from their adult hosts
have been shown to be important signals in locating eggs, related strains of a given host
plant species have different volatile profiles so that females of successful parasitoids
are capable of responding to more than one or a combination of cues. The specificity of
the components of the plantherbivore complex providing species-specific information
is an aspect deserving increased scrutiny. There are instar-specific blends of chemicals
emitted by faeces of second or fourth instar larvae and this is due to different digestive
processes of the larvae and the different microorganisms inhabiting the faeces. In some
cases as in Pieris brassicae volatiles from the hostplant complex do
not mediate discriminations of parasitoids between sites infested by young or old larvae;
but after landing on an infested leaf, the duration of searching is differently affected
by cues such as those of silk or frass related to the presence of the first or fifth
instar larvae37. Response to 7 or 8 carbon compounds by parasites is equally
high and a 1-carbon shift in the peak responses from 6 to 7 carbon compounds occurs in
frass so that the herbivore frass is a major source of 7-carbon compounds and of increased
parasite behaviour38. Such frass volatiles as linalool, guiacol and 3-octanone
mediating plant herbivorenatural enemy interactions in relation to the
soyabean looper Pseudoplusia includens were found to be the useful source of
information for the parasitoid Microplitis demolitor39.
Allelochemical influence on parasitoid fitness
The fitness of natural enemies is related to the
quality of hosts, which in turn is affected by plant nutrition and allelochemicals so that
the diversity and abundance of the hosts influence the diversity and abundance of natural
enemies40. Host plant nutritional characters indirectly alter the fitness of
parasitoids through change of herbivore quality41 and plants with digestibility
reducing substances support herbivory. Besides the influence of host physiology on the
fitness of parasitoids and the effects of plant physiology on the biology of natural
enemies, the effects of plant allelochemicals on parasitoid success and fitness are
essential aspects, since some of them may prevent normal nutrient use or cause inhibition
of enzyme systems42,43.
Some insects sequester toxic plant products and
actively metabolize and store the allelochemicals as defences against their natural
enemies, which in turn also separates them from their host insects. The transfer of a
plant toxin, say an alkaloid through a herbivore to a carnivore is also known. In
parasitoidhost relationship the future development of the host is important to the
parasitoid. While plant odours or floral scents attract or arrest natural enemies, some
relatively odourless crucifers produce enzymes in response to attacking insects that
quickly convert inactive mustard oils to volatile parasite-attracting derivatives44.
In such a situation a shift to a different plant may enable a phytophagous insect to
escape from parasitoids that use plant compounds as host-finding cues.
The stem borer Chilo partellus
produces volatiles attracting the parasite Cotesia flavipes and an exogenous
elicitor of this plant response has been identified in the regurgitate of the larva45.
b -galactosidase, as this elicitor is known, affects the production of attractants to the
natural enemies46. Of particular interest is the presence of anthraquinones and
anthrones in some chrysomelids. They not only act as feeding deterrents against predators,
but also influence a parasitoid to gain an evolutionary advantage by specialization on
such protected eggs, there being no transfer of these chemicals from the second to the
third trophic levels47. Although several plant-derived volatile compounds of
host plant origin play a significant role in natural enemy activity, several plant-derived
volatile compounds from trichomes also inhibit the activity of natural enemies, in
particular, 2-tridecanone and 2-undecanone which significantly alter cocoon spinning
behaviour48, aspects which may interfere with efficient biological control.
A comparison of volatiles of the frass of Helicoverpa
armigera indicates that larvae fed on artificial diet had no significant kairomonal
compounds like docosane and hexatriacontane, while the frass of H. armigera
fed on Abutilon and Gossypium plants indicated the presence of several
host-seeking kairomonal compounds that considerably influenced parasitoid behaviour.
Therefore the behaviour and success of natural enemies undergo considerable variations
when the herbivores colonize different host plant species in response to different
volatile compounds which modify the behavioural sequence of natural enemies49,50.
CottonHeliothisnatural enemy interactions
Extrafloral nectaries in cotton appear to be an
important source for parasitoids such as braconids, ichneumonids and trichogrammatids
involved in the control of bud worms and boll worms of cotton. These parasites are twice
as abundant in cotton cultivars with extrafloral nectaries which act as an energy source,
with sugars and varying types of aminoacids, increasing the longevity three to four times
of parasitoids like Trichogramma51. Trichogramma chilonis
showed increased parasitization of H. armigera eggs deposited on flowers and
young squares in view of the nectary source. Campoletis sonorensis and Microplitis
croceipes lived longer, exhibited higher fecundity and showed increased vigour in
nectaried cotton varieties, besides altering the physiological response of parasitoids52.
Several parasitoids show differential preference for various cotton cultivars due to the
availability of adequate kairomonal resource.
Volatile chemicals in cotton affect the behaviour of
parasitoids associated with the plant, a given chemical tending to act both as a plant
orientation compound or feeding stimulant or toxin for the herbivore. Members of other
trophic levels may be affected by chemicals through association with the plants and of the
chemicals and associated metabolites found in the body of their prey. Analysis of
volatiles of cotton cultivars in flowers, and squares revealed that in addition to their
nutritional quality, kairomonal compounds like tricosane and pentacosane act as attractant
resources for many of the parasitoids. Cotton gland chemicals also tend to influence
Parasitoids such as Campoletis sonorensis
antennate and probe cotton to a higher degree than other plants and cotton buds were more
extensively antennated and probed than leaves and stems and hence the importance of cotton
volatiles in providing host habitat location. Related species or strains of a given plant
would differ in attraction if the volatile profiles were altered. Gossypium barbadense
lacks myrcine, g -bisabolene, and b -bisabolol which are major components of G. hirsutum.
Typical gas chromatograms of volatiles of glanded cotton G. hirsutum showed
the presence of a -pinene, myrcene, ocimene, b -caryophyllene, a -humulene, g -bisabolene
and b -bisabolol. Individual compounds produced varying degrees of long-range attraction
and antennation upon contact. Caryophyllene oxide, a fragrant cotton sesquiterpene
attractant to C. sonorensis was also capable of reducing H. virescens
growth rate when added to the artificial diet gut in higher concentrations54.
Results of behavioural studies in response to five
cotton cultivars TCHB, Suvin, LRA, MCU 5 and MCU 7, indicated that the parasitoid Trichogramma
chilonis showed increased antennation and probing behaviour towards volatiles of
the cultivar Suvin compared to others. Gas chromatographic studies revealed the presence
of several volatile compounds such as docosane, caryophyllene, hexacosane and nonacosane
which significantly induced the behaviour of parasitoids. While caryophyllene has been
detected in the squares of Suvin, TCHB, MCU 7 and MCU 11, octodecane, undecane and
dodecane were identified in LRA. Tetradecenoic and hexadecenoic acids were typical of MCU
11. In many instances kairomones emanating from herbivores act alongside with host-finding
process. Volatile compounds emanating from the scales of Helicoverpa armigera
and Corcyra cephalonica moths were identified as hexatriacontane, docosane
and nonacosane which increased the activity of T. chilonis55,56.
Similarly kairomones from Helicoverpa eggs influenced the behaviour of T. chilonis
and the egg predator Chrysopa scelestes. The abdominal tip exudates of Spodoptera
litura females were identified as complex compounds containing dodecane,
heptadecane, octadecane and pentadecenoic acids which influenced the activity of the egg
parasitoid Telenomus remus57.
In response to herbivory, some plants release
volatile chemicals particularly attractive to parasites and one of the best documented
examples pertain to the spider mite Tetranychus urticae, its predator Phytoseiulus
persimilis and the host plant, which form a good example of tritrophic interactions58,59.
Cucumber plants infested by the spider mite release b -ocimene, and 4,8-dimethyl,
1,3,7-nonatriene, while lima beans releases a mixture of linalool, b -ocimene, the
nonatriene and methyl salicylate which are highly attractive. The volatiles released alert
uninfested neighbouring plants so that they become better protected from spider mite
attack. Cotton seedlings when infested by these mites release volatile cues which both
attract predatory mites and alert neighbouring plants to withstand herbivore attack.
Linalool released at the rate of 1 ng/hour before damage increased to
110 ng/hour six hours after the attack. In several other cases like the tritrophic
system in soyabean plant, involving Pseudoplusia and Microplitis molitor
and its parasites, besides linalool, other attractants like guiacol, 3-octanone from frass
have been noticed60.
The searching behaviour of
parasites and predators of herbivorous insects or phytophages, particularly information
from plants in their searching process indicates the importance of tritrophy. Plant
volatiles mediate searching behaviour at longer distances, not to mention of host insect
volatiles or herbivore-derived chemicals calling for a need to exploit the foraging
strategies of natural enemies for efficient biological control. The degree of insect
infestation is related to the value of plant information and induced defences greatly
increase emission of plant volatiles. The use of semiochemicals to enhance the behaviour
of biocontrol agents in agroecosystems holds great promise in future pest control
measures. Volatile chemicals promoting the behaviour of natural enemies as well as the
fact that the same chemicals affect the growth and survival of herbivores indicate that
manipulation of volatile profiles contribute significantly in biocontrol strategies. For
instance, compounds such as caryophyllene act as feeding deterrents and growth inhibitor
in Heliothis, while the same compound influences the searching efficiency of
natural enemies. Natural enemies have evolved the capacity to learn to use induced
responses to locate their hosts. Plants in turn use the third trophic level as another
line of defence against herbivores. Plants are therefore to be considered as a dynamic
component of insectplantnatural enemy interactions. The possibility of using
naturally occurring compounds from plants to reduce herbivore damage and increase the
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Received 1 February 1999; revised accepted 15 April