Integrated pest management: Looking back and forward

A. Sankaram

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 bookSilent 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 remedy.

Historical developments in pest control and management

Ascent of chemicals and pesticides

The forerunners of today’s 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 Tutankhamen’s 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 farmers.

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 decade’s 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 and pesticides

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 (1945–55). (ii) Confusion and the crisis of environment (1955–72). (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 1942–74 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 crop-production system.

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 (ICM).

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 methods.

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.

IPM components

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 prevented.
(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 population.

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 30’s. 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 self-perpetuating.

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 Spain.

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 imperative.

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. CIMMYT’s 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 insecticidal genes28.

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 world’s 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).31.gif (13767 bytes) 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 divisive insights.

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.


  1. Carson, R., Silent Spring, Penguin, London, 1962.
  2. Pimentel, D., Bull Entomol. Soc. Am., 1976, 22, 20–26.
  3. Pimentel, D., Socio-economic and Legal Aspects of Pest Control Strategies (eds Smith, E. H. and Pimentel, D.), Academic Press, New York, 1978, pp. 55–71.
  4. Metcalf, R. L., Annu. Rev. Entomol., 1980, 25, 219–256.
  5. Geier, P. W., Annu. Rev. Entomol., 1956, 11, 471–490.
  6. Bartlet, B. R., Agric. Chem., 1956, 11, 42–44.
  7. Stern, V. M., et al., Hilgardia, 1959, 29, 81–101.
  8. Lewis, W. J., et al., Proc. Natl. Acad. Sci. USA, 1997, 94.
  9. Allen, W. A. and Rajotte, E. G., Annu. Rev. Entomol., 1990, 35, 379–397.
  10. Bradfield, C. S. and Swisher, M. E., Food Rev. Intl., 1994, 10, 215–267.
  11. Smith, E. H., IPM: Insect Science and Its Application, 1983,
    vol. 4, Nos 1–2, pp. 173–177.
  12. Gooch, D., Chem. Ind., 1993, no. 6, p. 174.
  13. Corbet, P. S., Prot. Ecol., 1981, 3, 183–202.
  14. Morse, S. and William, B., IPM – Ideals and Realities, Lynne Rienner, Boulder, London, 1997, p. 180.
  15. World Resources Inst., World Resources, Oxford Univ. Press, New York, 1994.
  16. World Bank, IPM Strategies and Policies, Monograph Series No. 13, 1997.
  17. Van Huis, A. and Meerman, F., Int. J. Pest Manage., 1997, 43, 313–320.
  18. Rola, A. and Pingali, P., Agricultural Policy and Sustainability (ed. Faetf, P.), World Resources Inst., Washington DC, 1993.
  19. Paul, DeBach, Biological Control of Insect Pests and Weeds, Reinhold Pub. Corp, New York, 1964.
  20. Consultative Group of International Agricultural Research (CGIAR): 25 Year Annual Report, Washington DC, 1994.
  21. Watson, A. K., Curr. Adv. Herbicide Res., 1989, 3, 987–996.
  22. Gould, F., Bio-Science, 1988, 38, 26–33.
  23. Putman, A. R., Weeds, 1985, 2, 583–589.
  24. Hathway, D. E., Molecular Mechanisms of Herbicide Selectivity, Oxford Univ. Press, 1989.
  25. Winston, L., Mark, Nature Wars, Harvard Univ. Press, 1997.
  26. Evans, K. A. and Scarisbrick, D. H., Crop Protection, 1994, 13, 403–412.
  27. Hildeer, V. A. and Hamilton, W. D. O., Crop Protection in the Developing World, British Corporation Protection Council, 1994.
  28. Sane, V. A., Nath, P., Amiruddin and Sane, P. V., Curr. Sci., 1997, 72.
  29. Shantharam, S., Diversity, 1997, 13, 19.
  30. Andrew, C., Herbicide and Plant Physiology, Chapman and Hall, London, 1992.
  31. Luna, J. M. and House, G. J., in Pest Management in Sustainable Agricultural Systems, Soil Water Conservation Society, Ankeny, Iowa, 1990.
  32. Joshi, H. and Merril-Sands, D., ASM News, 1998, 64.
  33. UNEP, Beyond Silent Spring, Chapman & Hall, 1997.
  34. Barnard, C. M., Padgitt and Uri, N. D., Int. Pest. Control., 1997, 39, 161–167.


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.

Awareness of 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 faeces4–7, so that natural enemies base their foraging strategies on chemical information from the first and second trophic levels8–10. 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 distance15–17. 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.


Behavioural diversity

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 process30–32. Therefore, a close understanding of the intricacies of behavioural diversity of parasitoids appear essential in generating increased success in biological control programmes.

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 hosts34–36. 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 plant–herbivore 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 host–plant 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– herbivore–natural 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 parasitoid–host 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.

Cotton–Heliothis–natural 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 parasite biology53.

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 insect–plant–natural enemy interactions. The possibility of using naturally occurring compounds from plants to reduce herbivore damage and increase the effectiveness of biocontrol agents is a potential area for future research. In-depth studies of semiochemicals of plants and their role in natural enemy activity would enable screening and developing hybrid varieties that produce significant source of such chemicals for enhancing natural enemy activity.

  1. Price, P. W., Boethel, D. J. and Eikenbary, R. D., in Interaction of Plant Resistance and Parasites and Predators of Insects, Ellis, Harwood and Chichester, 1986, pp. 11–30.
  2. Price, P., Bouton, C. E., Gross, P., McPherson, B. A., Thompson, J. N. and Weis, A. E., Annu. Rev. Ecol. Syst., 1980, 11, 41–65.
  3. Craig, T. P. in Parasitoid Community Ecology, Oxford University Press, Oxford, 1994, pp. 205–227.
  4. Vinson, S. B., Annu. Rev. Entomol., 1976, 21, 109–133.
  5. Vinson, S. B. in Biological Control and Augmentation of Natural Enemies (eds Ridgway, R. L. and Vinson, S. B.), Plenum Press, New York, 1977, pp. 237–239.
  6. Vinson, S. B., in Semiochemicals and their Role in Pest Control (eds Nordulund, D. A., Jones, R. L. and Lewis, W. J.), John Wiley, New York, 1981, pp. 51–77.
  7. Vinson, S. B., in Comprehensive Insect Physiology, Biochemistry and Pharmacology (eds Kerkut, G. A. and Gilbert, L.), Pergamon Press, Oxford, 1985.
  8. Boethal, D. J. and Eikenbary, R. D., in Interaction of Plant Resistance and Parasitoids and Predator of Insects, John Wiley, New York, 1986.
  9. Steinberg, S., Dicke, M. and Vet, L. E. M., J. Chem. Ecol., 1993, pp. 47–59.
  10. Vet, L. E. M. and Dicke, M., Annu. Rev. Entomol., 1992, 37. 141–172.
  11. Orr, D. B. and Boethel, D. J., Oecologia, 1986, 70, 242–249.
  12. Agelopoulous, N. G., Dicke, M. and Posthumus, M. A., J. Chem. Ecol., 1995, 21, 1789–1811.
  13. Karban, R. and Baldwin, I. T., Induced Responses to Herbivory, The University of Chicago Press, Chicago, 1997, p. 319.
  14. Agelopoulous, N. G. and Keller, M. A., J. Chem. Ecol., 1994, 20, 1725–1734.
  15. Benray, B., Denno, R. F. and Kaiser, L., J. Insect Behav., 1997, 10, 619–629.
  16. Turling, T. C. J. and Tumlinson, J. H., Fl. Ent., 1991, 74, 42–50.
  17. McCall, P. J., Turlings, T. C. J., Lewis, W. J. and Tumlinson,
    J. H., J. Insect Beh., 1993, 6, 625–639.
  18. Vet, L. E. M. and Groenewold, A. W., J. Chem. Ecol., 1990, 16, 3119–3135.
  19. Edward, P. J. and Wratten, S. D., Oecologia, 1993, 59, 88–93.
  20. Annadurai, R. S., Murugesan, S. and Sen Rayan, R., Proc. Indian Acad. Sci. (Anim. Sci.), 1990, 99, 317–325.
  21. Dicke, M. and Sabelis, M. W., Netherlands J. Zool., 1988, 38, 148–165.
  22. Faeth, S. H., in Parasitoid Community Ecology (eds Hawkin,
    B. A. and Sheehan, W.), Oxford University Press, Oxford, 1994, pp. 245–260.
  23. Nordlund, D. A., Jones, R. L. and Lewis, W. J., Semiochemicals: Their Role in Pest Control, John Wiley, New York,1981.
  24. Whitman, D. W., in Novel Aspects of Insect–Plant Interactions (eds Barbosa, P. and Letourneu, D. K.), John Wiley, New York, 1988, pp. 11–64.
  25. Whitman, D. W. and Eller, F. J., Chemoecol., 1990, 1, 69–75.
  26. Price, P. W., Biol. Control, 1991, 1, 83–93.
  27. Vet, L. E. M. and Dicke, M., Annu. Rev. Entomol., 1992, 37, 141–172.
  28. Mattiacci, L. and Dicke, M., J. Insect Beh., 1995, 8, 485–498.
  29. Noldus, L. P. J. J. and Van Lentern, J. C., J. Chem. Ecol., 1985, 11, 783–791.
  30. Lewis, W. J., Jones, R. L. and Nordlund, D. A., Behav. Biol., 1976, 16, 267–289.

  31. Vinson, S. B., in Insect Communication (eds Trevor Lewis), Academic Press, London, 1989, pp. 379–400.

  32. Nortlund, D. A., in Biological Control with Egg Parasitoids (eds Wajnberg, W. and Hassan, S. A.), CAB International, London, 1994, pp. 155–163.
  33. Hare, D. J., in Plant Resistance to Herbivores and Pathogens: Ecology, Evolution and Genetics (eds Fritz, F. S. and Simms,
    E. L.), University of Chicago Press, 1992, pp. 278–300.
  34. Barbosa, P. and Letourneau, Novel Aspects of Insect–Plant Interaction, John Wiley, New York, 1988, p. 285.
  35. Geervliet, J. B. F., Vet, L. E. M. and Dicke, M., Ent. Exp. App., 1994, 73, 289–297.
  36. Vinson, S. B. and Iwantsch, G. F., Annu. Rev. Entomol., 1980, 25, 397–419.
  37. Mattiacci, L. and Dicke, M., J. Insect Behav., 1995, 8, 485–498.
  38. Ramachandran, R. and Norris, D. M., J. Chem. Ecol., 1991, 17, 1665–1690.
  39. Ramachandran, R., Norris, D. M., Phillips, J. K. and Phillips,
    J. W., J. Agric. Food Chem., 1991, 39, 2310–2317.
  40. Dicke, M., Sabelis, M. W., Takabayashi, J., Bruin, J. and Posthumus, M. A., J. Chem. Ecol., 1990, 16, 3091–3118.
  41. Ananthakrishnan, T. N., Curr. Sci., 1990, 59, 1319–1322.
  42. Ananthakrishnan, T. N., Curr. Sci., 1991, 70, 215–218.
  43. Schoonhoven, L. M., Jermy, T. and van Loon, J. J. A., Insect–Plant Biology, Chapman and Hall, London, 1998, p. 409.
  44. Panda, N. and Khush, G. S., Host Plant Resistance to Insects, CAB International, Wallingford, 1995, pp. 96–101.
  45. Potting, R. J., Vet, L. E. M. and Dicke, M., in Novel Aspects of Insect–Plant Interaction (eds Barbosa, P. and Letourneau D.), John Wiley, New York, 1988, pp. 65–90.
  46. Mattiacci, L. and Dicke, M., J. Insect Behav., 1995, 8, 485–
  47. Meiners, T., Kopf, A., Stein, C. and Hilker, M., J. Insect Behav., 1991, 10, 523–539.
  48. Kaufmann, W. C. and Kennedy, G. G., J. Chem. Ecol., 1989, 15, 2051–2060.
  49. Ananthakrishnan, T. N. and Senrayan, R., Phytophaga, 1992, 4, 87–94.
  50. Lewis, W. J. and Martin, W. R., J. Chem. Ecol., 1990, 16, 3067–3089.
  51. Pemberton, R. W. and Lee, J. H., Am. J. Bot., 1996, 83, 1187–1194.
  52. Eizen, G. W., Williams, H. J. and Vinson, H. B., Environ. Ent., 1983, 12, 1873–1877.
  53. Williams, H. J., Elzen, D. W. and Vinson, S. B., in. Novel Aspects of Insect–Plant Interaction (eds Barbosa, P. and Letourneu, D. K), John Wiley, New York, 1998, pp. 171–200.
  54. Barbosa, P. and Saunders, J., in Chemically Mediated Interaction Between Plants and Other Organisms (eds Driver, G. A. C., Swain, T. and Conn. E. E.), Plenum Press, New York, 1985, pp. 107–138.
  55. Ananthakrishnan, T. N., Senrayan, R., Murugesan, S. and Annadurai, R. S., J. Biosci., 1991, 16, 111–119.
  56. Annadurai, R. S., Murugesan, S., Senrayan, R., Guru Subramanian, G. and Ananthakrishnan, T. N., in Emerging Trends in the Biological Control of Insects (ed. Ananthakrishnan, T. N.), Oxford and IBH, New Delhi, 1990, pp. 83–101.
  57. Ananthakrishnan, T. N. and Senrayan, R., Phytophaga, 1992, 87–94.
  58. Bruin, J., Dicke, M. and Sabelis, M. W., Experientia, 1992, 48, 525–529.
  59. Margolis, D. C., Sabelis, M. W. and Boyer, J. E., J. Insect Behav., 1997, 10, 695–709.
  60. Moraes, De, C. M., Lewis, W. J., Pare, P. W., Alborn, S. T. and Tumlinson, J. H., Nature, 1998, 393, 570–574.

Received 1 February 1999; revised accepted 15 April 1999