AUGMENTIVE & INUNDATIVE STRATEGIES
WITH NATURAL ENEMIES
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Inundative releases of natural enemies to augment activity in the field and to improve pest control have been practiced for many years (King et al. 1985a, Kogan et al. 1999). Annual short term crops are particularly suited for the inundative release approach in biological control, because they often fail to provide a stable environment for the continuous abundance of natural enemies. By manipulating the kinds of natural enemies, the stage of their development for release, the numbers released and the time and modes of release, a much more active role is required of field managers than in classical biological control. Kogan et al. (1999) showed that successes of inundative releases may depend upon (1) the nature of the crop plant, (2) the developmental stage of the crop, (3) the developmental stage of the pest, (4) the absolute density of pest organisms, (5) the quality of the natural enemies, including host specificity, searching capacity and proper identity, (6) the density of natural enemies, (7) the climate, (8) complementary or antagonistic effects of other natural enemies, (9) ability to integrate releases with other control methods, particularly insecticides, and (10) the cost of the release program. Five examples of inundative or inoculative release programs will represent the range of crop/pest systems and spectrum of natural enemies for which augmentation has adopted.
Trichogramma spp. For Annual Crops.
Trichogramma species are presently the most widely used insects in inundative and augmentive control (Ridgway & Morrison 1985). The area of crops covered by Trichogramma releases has increased annually and amounts to ca. 11 million ha. in the former Soviet Union (Voronin 1982), 5,500 ha. in Western Europe (Hassan et al. 1986), 355,000 ha. in the United States and about 2 million ha. in the People's Republic of China (van Lenteren 1987), and extensive areas in Mexico (Jimenez 1980). Annual crops on which Trichogramma are used include rice, crucifers, sorghum, millet, sugar beets, cotton, corn and cassava. However, documentation of the release data and the outcomes of release programs are mostly lacking, which makes it difficult to evaluate results and to draw conclusions about the applicability of particular practices to the overall use of Trichogramma for biological control. Consequently, a scientific discussion is limited to a few prominent examples.
Trichogramma in Cotton.--Cotton, Gossypium hirsutum, is a perennial plant that is usually grown as a warm season annual. In the Northern Hemisphere it is typically planted in March or April and, according to the variety, harvested between August and November. The plant is attacked by many insects, particularly Homoptera, Hemiptera and Lepidoptera, from germination to picking time (Reynolds et al. 1982). However, the early season, which is typified by vigorous plant growth, is often characterized by a relatively smaller risk of insect damage than is the later part of the season. This is because of the relatively high abundance of natural enemies in the early part of the season (Bar et al. 1979), to the lower susceptibility of plants to damage because no mature fruits are present and because of their capacity for compensatory growth (Wilson 1986a), and the lower numbers and less damaging characteristics of many early season pests. Therefore, the use of early season insecticide treatments in cotton is particularly unnecessary and its avoidance may enable growers to extend substantially the insecticide-free period of the crop.
Trichogramma pretiosum (Riley) and T. australicum Girault are used in Colombia to control early season lepidopterous cotton pests such as Alabama argillacea (Hübner), Trichoplusia ni (Hübner), Pseudoplusia includens Walker, Sacadodes pyralis Dyar and Heliothis spp. (Amaya 1982). Releases are intended to prevent damage by these pests and to facilitate an insecticide-free period of about 100 days, after which treating against boll weevils, Anthonomus grandis Boheman is often necessary (Kogan et al. 1999). The parasitoids are mass reared on Sitotroga cerealella Zeller, mostly in local insectaries and released in the field as pupae within host eggs that are glued to small (6 cm2) cardboard strips, each bearing 3,000 eggs, 85% of which are parasitized. Releases start 20-25 days after germination and continue throughout the season. The first three releases are made at five day intervals to establish an overlapping parasitoid population. Subsequent releases are made every eight days. Each release consists of 20 cards (ca. 51,000 parasitoids) up to square formation, and 30 cards (ca. 76,000 parasitoids) thereafter (Amaya 1982). Sometimes parasitoid releases may begin at planting time when parasitoids are liberated along field margins to kill Lepidoptera that develop on the surrounding vegetation, and continue within the field at about weekly intervals for some three months. Parasitoids are released as freshly emerged adults, first at the rate of 40-50,000 per ha. and later 30-36,000 per ha. The exact timing of releases is determined by field scouting performed twice weekly by the growers (Kogan et al. 1999). When unavoidable insecticide applications occur, Trichogramma releases are made as soon as two days after applications to maintain continuous control (Amaya 1982).
Inundative programs using Trichogramma resulted in a marked reduction of insecticide treatments. In a 15,000 ha. area of the Valle del Cauca, Colombia, the number of treatments changed from 20 per year in 1975 to four in 1981; on 6,000 ha. in the norther part of that region, the number was reduced to 1.2 treatments per year. The success in Colombia and in Mexico is due partly to the relatively inexpensive and efficient Trichogramma production methods available. However, emphasis on applied research for the improvement and maintenance of parasitoid quality through continuous selection, the development of parasitoid storage techniques, the accurate determination of the quantities of parasitoids to be released and the correct timing of the releases have been crucial to the success of the program (Amaya 1982, Kogan et al. 1999).
In the former Soviet Union, special races of T. euproctidis Girault are used for the control of Heliothis armigera Hübner and of cutworms, Agrotis sp. in Central Asian cotton (Voronin 1982). In the case of H. armigera, three releases of the parasitoids at the rate of 1:1 or 1:2 pest:parasitoid are used with a resulting parasitism of 66-90%. Release rates against cutworms are 200,000 per ha., three times, once every 5-7 days when cotton is in the seedling stage. This procedure provides complete protection of the crop. Release thresholds in Tadjikistan against H. armigera are such that only 50% parasitization efficiency is sufficient for economic control (Voronin 1982).
In the People's Republic of China about 680,000 ha. of cotton are treated with Trichogramma (Huffaker 1977). In over 100,000 ha. of the Shaanxi Province, control of Heliothis is achieved with the release of T. chilonis Ishii ( = T. confusum Viggiani). The parasitoids are applied at the rate of 120,000 per ha. in a total of three releases at 3-4 day intervals during the F2 host generation; 75% parasitization is achieved (King et al. 1985b). In the Jiangang farm, H. armigera has been controlled on 3,546 h. yearly between 1975-1984 by releasing 414,000 parasitoids/ha. Parasitization reaches 45% with a residual worm density of 4/100 plants. The large amount of data obtained permitted the construction of a reliable model for predicting the efficiency of T. confusum in cotton fields during the third and fourth host generations (Zhou 1988).
Studies on the practicality of using Trichogramma species, especially T. sp. nr. pretiosum for the control of the bollworms H. zea and H. virescens have been conducted in the United States (King et al. 1985c). A three-year pilot test was conducted in southeastern Arkansas in 1981 and North Carolina in 1983 to evaluate Trichogramma for controlling Heliothis species in cotton King et al. (1985b) summarized the project and its achievements and concluded that mean parasitism rate of 47.4% of Heliothis spp. by T. sp. nr. pretiosum augmented in cotton was insufficient to provide adequate control (King et al. 1985c). Explanations for the failure of Trichogramma in the United States were presented in contrast to its successes in China, South America and Mexico. A key reason was the higher production cost of the parasitoids in the United States, especially compared to the lower cost of insecticides. Low insecticide costs in the United States also create lower economic thresholds for Heliothis, which in turn promote numerous insecticide treatments. An additional factor that plays an important role in many other areas of the world where cotton is grown, is the frequent need to use insecticides against other pests, with the result that such treatments further disrupt parasitoid performance.
Trichogramma in Corn.--Corn, Zea mays, is an annual crop that, like cotton, is grown during the warm season of the year. The growth cycle from planting to harvest varies from two to five or six months according to the variety and growing conditions. Corn originated in the Western Hemisphere and has spread worldwide (Aldrich et al. 1975). It has become a cosmopolitan staple. In addition to the indigenous pest complex on corn, many local insect species have adapted to the crop, and presently each geographic region has both cosmopolitan and local corn pests (Chiang 1978).
The European corn borer, Ostrinia nubilalis Hübner, originally fed on unknown hosts, but readily moved onto corn, spreading from Europe to reach the status of a severe pest of worldwide importance in temperature and cold climate countries (Balachowski 1951, Kogan et al. 1999). Along the northern boundaries of its distribution in Germany, Switzerland and the former Soviet Union, China and Canada, the corn borer has only one generation per year. Here it may be the main or only serious corn pest (Hassan 1982). The number of generations per year increases at lower latitudes just as the complex of pests associated with corn expands. Therefore, insecticide treatments against the corn borer in its univoltine range are not only expensive and environmentally disruptive but may cause the outbreak of secondary pests such as aphids, which would otherwise be controlled by natural enemies (Hassan 1982). Efforts to control the corn borer by releasing Trichogramma were first reported from the former Soviet Union (Zimin 1935) and such efforts have continued ever since (Voegele 1988). However, commercial efforts to use Trichogramma were initiated only during the last decade after successful field trials were carried out in Europe (Bigler 1986, Voegele 1988). The number of countries using commercial Trichogramma rose within a few years from two (former Soviet Union and People's Republic of China) to 10 (Austria, Bulgaria, Colombia, France, Italy, Germany, Switzerland and the United States).
Several reasons propelling the commercial use of Trichogramma as a principal means of corn borer control are (1) concern over the disadvantages of chemical pesticides, (2) increase in the efficiency of Trichogramma production, (3) awareness of the importance of the specific biological characteristics of the parasitoid to be used, leading to the acquisition of more efficient parasitoid species (Beglyarov & Smetnik 1977, Huffaker 1977, Bigler et al. 1982, Voronin 1982, Hawlitzky 1986, Voegele 1988), and (4) identity of the requirements for optimal field releases (Stengel 1982, Voronin 1982, Hassan et al. 1986, Hawlitzky 1986).
Most researchers maintain that parasitoids must be in the field before the first oviposition wave of corn borer, and various methods have been devised to accomplish this. Hassan et al. (1986) used light traps to detect the first appearance of adult moths. In France, Stengel (1982) and Hawlitzky (1986) discuss a day-degree calculation based on records of the development and flight of the moths since 1963. These data, together with the emergence of moths from caged pupae, are used to determine the onset of oviposition. Economic threshold is reached when 10-12% of the eggs have been laid about three weeks after first flight. This threshold varies according to climatic conditions and corn variety, ranging from 6% for early and 15% for late varieties.
Inclement weather and predators may cause mortality of the parasitized eggs that are placed in the field. Egg predation becomes more severe with longer exposures. Methods are available to minimize such mortality factors. In France, Hawlitzky et al. (1987) placed parasitized eggs in specially designed perforated capsules 1-3 days before emergence. In Germany Hassan (1982) placed egg cartons within a 3 x 6 cm screen saran bag as protection against predators and a plastic cover as protection against rain. In the People's Republic of China plastic bags are employed (Coulson et al. 1982).
It is especially important to guarantee the quality of parasitoids, as was demonstrated by a reduction of parasitism from 75.2% in 1978 to 18.8% in 1979 in Switzerland when mass produced wasps deteriorated (Bigler et al. 1982). Stock quality is usually assured by rearing at least one generation annually on O. nubilalis eggs (Bigler et al. 1982, Hassan 1982, Voronin 1982). Stock can also be strengthened by introducing field collected material, a practice that is very common in the People's Republic of China (Coulson et al. 1982). Voegele (1988) discussed the preservation of stock quality through the retention of original traits and improvement of parasitoids. He recommended that in addition to the cyclic return to natural hosts, to use isogenic females, manipulate the nutrition of the parasitoids in artificial rearing media, optimize the host/parasitoid ratio in culture, manipulate parasitoid diapause, use semiochemicals from the plant or from the host insect, and select for insecticide resistance. Kogan et al. (1999) suggested that genes for insecticide resistance as well as genes for response to certain environmental stimuli may also be introduced into the parasitoid cultures.
Other Crops.--In the former Soviet Union Trichogramma was used to control lepidopterous pests of peas and cabbage. Parasitization of 89-96% of the eggs of Laspereysia dorsana F. and 67% of the eggs of Autographa gamma L. attacking peas was achieved following the enrichment of the environment with nectariferous plants (e.g., Phacelia tanecetifolia). The use of nectar sources marked an improvement over the 29 and 31% control that had been obtained without those sources, largely because of increased parasitoid longevity. Similar results were obtained in the control of A. gamma on cabbage, where improvement was from 50-60% to 80-90% parasitization (Voronin 1982). Noctuid larvae that infest sugar beets and potatoes were controlled by releasing 20-60,000 parasitoids per ha., which resulted in a 60-90% reduction in infestation levels (Beglyarov & Smetnik 1977).
The rice leaf roller, Cnaphalocoris medinalis Guenee, and other rice pests are controlled in the People's Republic of China by five seasonal releases of from 150,000 to 600,000 T. australicum per ha., depending on the host density (Kogan et al. 1999). The resulting parasitism amounts to 80% and the total cost is half that for insecticidal control (Huffaker 1977).
Shen et al. (1988) reported successful results with inoculative releases of only 15,000 T. dendrolimi per ha. on seven experimental hectares of rice. In Colombia Trichogramma is used for the biological control of various crop pests in addition to those on cotton and corn. These include beans and soybeans, where the pests are Anticarsia gemmatalis and Heliothis sp. and cassava, where the principal pest is the sphingid moth Enrinnyis ello (L.). Parasitoids are released on egg cards at the rate of 51,000 per ha from 10 days after germination for beans, and 76,500 per ha. starting 30 days after plant emergence for cassava. Initial releases were spaced five days apart; later releases eight days apart, and satisfactory control was reported (Amaya 1982).
Spider mites have been controlled biologically for over two decades with considerable success (Huffaker et al. 1970), with most work involving glasshouses (see section on glasshouses). Outdoor crops are either treated with acaricides or efforts are made to conserve naturally occurring predatory mites (Jeppson et al. 1975). The active suppression of spider mites in fields was studied by Oatman et al. (1976, 1977a, 1981), who used three species of phytoseids, Amblyseius californicus (McGregor), Phytoseiulus persimilis Athias-Henriot, and Typhlodromus occidentalis Nesbit to suppress Tetranychus urticae Koch in California strawberry fields. Phytoseiulus persimilis was the most efficient of the three predatory species. This predator was successfully established in southern California where it survived in strawberry and lima bean fields as well as on weed species in the genera malva, Solanum, and Convolvulus. The weeds served as reservoirs for the predators, from which they dispersed to strawberry and lima beans during the season. However, in most cases the economic thresholds in these crops were too low to enable a complete reliance on these predators for control (Oatman et al. 1981).
In Israel, the Netherlands and France, commercial use of inundative predatory mite releases in open fields has been practiced effectively. In Israel, spring melons, cantaloupes and watermelons grown in the Jordan and Arava Valleys, have been subjected each season to attacks by T. cinnabarinus (Boisduval) and T. urticae. The normal practice of using acaricides against these mites was expensive and in many cases insufficient due to an increase in resistance. This enabled commercial companies to culture A. persimilis for inundative releases. Fields are surveyed every week for germination, and predatory mites are released when spider mites are found. The release rate is 20,000 predators per ha. or about one predator to 10 spider mites when the plants are at the four leaf stage and double that amount when plants are larger and have formed runners. This method has the disadvantage of dispersing predators evenly throughout the field, whereas spider mites are usually found in aggregates. The result is that local epizootics may occur, and the introduction of additional natural enemies may be required. The problem can be circumvented with preemptive releases of a mixture of 5/1 spider mites/predators in fields not yet infested (Kogan et al. 1999). Biological control in Israel has resulted in an average net savings of ca. $300 per ha, and growers experienced better yields due to the absence of phytotoxic pesticides and a reduction in soil compaction that had been caused earlier by ground spraying equipment. Aphid attacks were also substantially reduced.
The commercial control of T. urticae in vegetable crops through the release of P. persimilis has been gaining acceptance in France and The Netherlands. The system is based on the integration of pesticide treatments against diseases and thrips and on two widespread releases of 4-5 predaceous mites per m2. Treatments against thrips with mevinphos are made two days before the first mite release about 2-3 weeks after planting. Treatments are accompanied by inspection and monitoring of infestation levels. Infestations usually decline below the economic injury level following the second release. This system is integrated with treatments against Botrytis, mildew and Pseudoperenospora and it has been applied successfully to strawberries in France and to strawberries and pickling cucumbers in Holland. The major advantages are healthier and stronger plants that last longer and extend the growing season (Kogan et al. 1999).
In cassava there have been reported about 50 species of phytophagous mites, in the genera Tetranychus and Mononychellus, which are particularly destructive both in South America and in Africa, mainly when they reach high infestation levels during dry seasons (Bellotti et al. 1982, Mesa & bellotti 1987). The South American species Mononychellus tanaioa (Bondar), or cassava green mite, was first detected in east Africa in 1971 (Bellotti & Schoonhoven 1978, IITA 1987a). It spread rapidly throughout most cassava-growing areas of Africa. The green mite seems to be specific to species of Manihot and a few other Euphorbiaceae. Yield losses range from 13 to 80 percent, mainly as a result of defoliation (IITA 1987a). Bellotti & Schoonhoven (1978) report several predators feeding on cassava mites, including coccinellids of the genera Stethorus, Chilomenes and Verania; the staphylinid Oligota minuta; the anthocorid Orius insidiosus; several species of cecidomyiids and thrips; and the phytoseid mites, Typhlodromalus limonicus, and T. rapax. The phytoseid mites and Oligota minuta seem to be the predominant predators. Later studies showed that some 19 species of predaceous mites were present in cassava fields infested by the green mite in Colombia (Bellotti et al. 1982, Mesa & Bellotti 1987).
A comprehensive biological control program of the cassava green mite complex in Africa involves cooperation among national and international research centers. According to this plan, five species of predaceous mites, Typhlodromalus limonicus, Neoseiulus anonymus, N. idaeus, Galendromus annecteres, and Euseius concordis are mass produced at CIAT, Colombia, on Mononychelus progressivus with a method that was developed by Mesa & bellotti (1987). Predaceous mite shipments are routed through CIBC quarantine in London and then forwarded to Africa for field release. This biological control effort, coupled with the propagation of resistant cassava varieties and cultural control methods are expected to alleviate the impact of the green mites on cassava in Africa (IITA 1987a, Kogan et al. 1999).
The Mexican bean beetle, Epilachna varivestis Mulsant, has been under a control program that involves inoculation releases of an imported parasitoid. Importation of the tachinid Aploymyiopsis epilachnae (Aldrich) from Mexico during 1922-1923 was the first attempt to control this beetle on common bean, Phaseolus vulgaris L. (Smyth 1923, Jones et al. 1983). The parasitoid failed to become established despite extensive releases of the flies in 19 states. Although as much as 90% parasitization was attained the fly could not survive the winter (Landis & Howard 1940). Importations specifically aimed at controlling this beetle on soybeans were made in 1966 when two parasitoids of Oriental species of Epilachna were brought from India (Angalet et al. 1968). The egg parasitoid Tetrastichus ovulorum Ferriere did not adapt to the new host, but the eulophid Pediobius foveolatus (Crawford), a larval-pupal parasitoid, selectively attacked E. varivestis but not the larvae of beneficial coccinellids. Although the parasitoid produced various generations with a season, thereby attaining high levels of parasitization, it could not overwinter in the central United States.
Inoculative releases were begun on an areawide basis in 1974, based on the establishment of nurse crops of common bean (Stevens et al. 1975b). Patches of common bean were strategically established early in the growing season in areas adjacent to soybean fields. The Mexican bean beetle was attracted to the bean patches and established healthy colonies that served as breeding hosts for P. foveolatus kept over the winter in laboratory colonies (Stevens et al. 1975a). From these patches the parasitoids readily spread to soybean fields where levels of parasitization remained between 60-90%. The program is presently conducted in Maryland, Delaware and Virginia (Schultz & Allen 1976) and has been tested in South Carolina (Shepard & Robinson 1976).
Pediobius foveolatus releases in central Florida in 1975 and 1976 reduced Mexican bean beetle populations to barely detectable levels in commercial fields, although in home gardens, common beans continued to be damaged. The success of the parasitoid in Florida has been attributed to the long growing season that allows up to 10 generations of the parasitoid. Additionally there is an abundance of beggar weed, Desmodium tortuosum, a preferred wild host of the beetle that serves the natural inoculum of the parasitoid (Jones et al. 1983, Kogan et al. 1999). This program is an example of the use of a nurse crop in connection with inoculative releases of a parasitoid originally obtained from a host species different from that of the species targeted for biological control. The economic feasibility of the program has been demonstrated (Reichelderfer & Bender 1979). Current research focuses on strains of P. foveolatus imported from Japan (Honchu) at latitudes comparable to those in regions of the United Sttes affected by the Mexican bean beetle, but no new strains have thus far overwintered (Jones et al. 1983).
Microbial Pesticides For Short Term Crops
Microbial agents that have been investigated for controlling pests in short term crops include entomopathogenic viruses, bacteria, fungi and protozoa. Although many pathogens have shown promise in field trials, very few microbial insecticides are commercially available for use on short term crops.
Bacillus thuringiensis, the spore-forming bacterium, is the most widely used microbial insecticide. It produces a toxic crystal at the time of sporulation that is very active against Lepidoptera, but also safe to humans and natural enemies. The insect for mortality to occur must ingest the crystal. Burges & Daoust (1986) estimated that total annual sales in the United States were $40 million, most of which were used to control forest Lepidoptera. As about 50 percent of all insecticides used in the United States are applied to cotton, it might be expected that B. thuringiensis would be used extensively on that crop, which it is not. Control has been too unreliable and variable, probably because Heliothis spp. and Pectinophora gossypiella, major cotton pests, bore into squares and bolls before ingesting enough of the leaf surface to cause mortality. Vegetables sustain the greatest use of B. thuringiensis. In 1985 between $5-10 million was spent on this bacterium for the control of Plutella xylostella (L.), Artogeia rapae (L.) and Trichoplusia ni (Hübner). A portion of the genome, which produces the toxic crystal of B. thuringiensis, has been incorporated into other bacteria and in higher plants. Very recent information (1999) on the effectiveness of the toxin applied in the manner in plants is that it is not as toxic as when applied directly to plant surfaces. There is even some evidence that when incorporated into the genome of potatoes, it causes illness in humans who consume the tubers (P. Maddon, pers. commun.).
No commercial fungal products are available for insect pests of annual crops in the United States, but government-sponsored mass production of Beauveria bassiana is prevalent in the former Soviet Union, primarily for control of the Colorado potato beetle. Species of Metarhizium have been extensively tested for the control of planthoppers in sugarcane and pasture grasses in Brazil (Kogan et al. 1999). Although many additional fungi have been field-tested, there is no commercial availability expected in the near future.
Kogan et al. (1999) report that with the emphasis on lepidopteran defoliators of soybeans, three strategies have been considered in the experimental development of Nosema rileyi as a biological control agent: (1) inundative releases (Getzen 1961, Mohamed 1978), (2) induced epizootics (inoculative releases) (Sprenkel & Brooks 1975, Ignoffo et al. 1976), and (3) manipulation of the ecosystem (Sprenkel et al. 1973). However, it is doubtful that N. rileyi will ever be used extensively as a microbial insecticide. Ignoffo (1981) listed characteristics of this microsporidian that limit its success as a microbial insecticide: (1) it kills slowly, allowing older caterpillars to cause considerable damage before dying, 92) it requires free water for germination, growth and sporulation, (3) it has a temperature requirement of 15-30°C, and extreme field temperatures may limit its effectiveness, and (4) to be effective large spore dosages must be directed at young insects.
Carner & Turnipseed (1977) isolated a nuclear polyhedrosis virus from larvae of Anticarsia gemmatalis collected in southern Brazil. the virus was imported into the United States and examined for pathogenicity. Small plot field tests gave significant reductions of A. gemmatalis, which were confirmed in Florida by Moscardi (1977). Since the early 1980's extensive field and laboratory studies were continued in Brazil (Moscardi & Correa Ferreira 1985). The virus (AgNPV) is highly specific to A. gemmatalis (Moscardi & Corso 1981) and is effective at field dosages above 10 LE/ha. Populations are reduced below the economic injury level with a single application of the virus suspension, and mortality soars to 80% at 40 LE/ha. (Moscardi 1983). Leaf consumption by diseased larvae was reduced by about 75% and although the half-life of crude preparations or a purified preparation with a clay adjuvant was either six or seven days, respectively, a single application was sufficient to control the caterpillars (Moscardi 1983).
Kogan et al. (1999) report that large-scale field testing with this virus started in Parana during 1980. The virus was applied as a crude preparation at 50 LE/ha. when A. gemmatalis larvae were less than 1.5 cm long. Applications were made with ground equipment at rates of 100-200 L of water per ha. Virus used in the field experiments were extracted from batches of 50 cadavers of large caterpillars (>2.5 cm). The dead larvae were macerated in water and filtered through several layers of cheesecloth. The suspension was then transferred to a sprayer tank containing the amount of water needed to cover one ha. Infectivity after four days was 80%. Experiments were conducted in areas of high incidence of A. gemmatalis and check plots were either treated with standard insecticides or left untreated. In all cases, yields were as high with the virus treatment as they were with insecticides (Moscardi 1983). An estimated 11,000 ha. of soybeans were treated with the virus in 1983 and the area was expected to increase to 300,000 ha. in 1984 (Moscardi & Correa Ferreira 1985).
At the present time there is only one virus available as a commercial produce in the United States, which is the nuclear polyhedrosis virus of Heliothis zea. Field trials have been conducted on control of insect pests of short term crops with many different baculoviruses. Many of these trials have produced encouraging results, but the costs of production make large-scale commercialization difficult. Many of these viruses can best be produced in a cottage industry environment and in areas where hand labor is inexpensive (Kogan et al. 1999).
The IPM approach most compatible with biological control is the development of plant resistance (Kogan 1982). Nevertheless, incompatibilities arise when mechanisms of resistance indiscriminately affect both pests and natural enemies, or when natural enemies are indirectly affected through their hosts or prey. Experimental evidence of incompatibilities is shown in tomato (Duffee & Isman 1981, Duffey & Bloem 1986, Duffey et al. 1986). This may be illustrated with Heliothis zea, Spodoptera exigua and the endoparasitic wasp, Hyposoter exiguae (Vier.). When host larvae ingest a diet with the glycoalkaloid tomatine, the development of the parasitoid is detrimentally affected (Duffey & Bloem 1986). Kogan et al. (1999) warn that such studies demonstrate that depending on the mechanism of resistance, natural enemies may be detrimentally affected; and that when exploiting such mechanisms one should weigh the risk of reducing the natural enemy load versus the benefit of the particular resistance trait.
Obrycki (1986) studying the impact of potato glandular trichomes on Edovum puttleri (Grissell, an egg parasitoid of the Colorado potato beetle, drew similar conclusions. He showed that E. puttleri readily parasitizes L. decemlineata eggs on Solanum tuberosum but that the parasitoid is entrapped in glandular trichomes of Solanum berthaultii. On S. tuberosum, egg mortality is increased not only due to parasitism but probably also to host feeding and superparasitism. But aphid parasitoids that are equally affected by S. berthaultii trichomes in the greenhouse were not greatly affected in the field, showing that moderate levels of trichomes and the biological control of potato aphids are not incompatible. Therefore, it is apparent that both biochemical and physical plant defenses are potentially detrimental to natural enemies. As behavioral adaptations of parasitoids of insects adapted to resistant lines may occur in nature, it would be useful to identify such adapted populations when searching for new sources of natural enemies (Kogan et al. 1999).
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