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BIOLOGICAL CONTROL OF ARTHROPODS

IN ROW & SHORT-TERM CROPS

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Introduction	Cereal Leaf Beetle, Oulema melanoplus
Dynamics in Short Term Crops	Alfalfa Weevil, Hypera postica
Natural Control in Short Term Crops	European Corn Borer, Ostrinia nubilalis
Classical Biocontrol in Short Term Crops	Cassava Mealybug in Africa--Phenacoccus manihoti
Southern Green Stink Bug, Nezara viridula	References
Melon Fly, Dacus cucurbitae	[Please refer also to Related Research ]

Introduction

Biological control is most successful when used in stable perennial agroecosystems (DeBach 1965, Huffaker & Messenger 1976, Luck 1981, Price 1981, Hokkanen 1985). Annual cropping systems are generally too unstable to sustain delicate tritrophic level interactions (Kogan et al. 1999). When the natural control of pest species has been upset by cultural operations and chemical pest control, adequate levels of biological control are difficult to restore. Yet, probably the majority of human food is produced from crops that are annual or short term, and therefore deserve maximum attention for alternatives to routine insecticide application. Many annual crop ecosystems benefit from a high level of natural control, in particular when an ecosystem has not been invaded by exotic pests that require the use of disruptive insecticides (Wilson 1985). Turnipseed & Kogan (1983) suggested that indigenous natural enemies are important in the regulation of minor phytophagous pests, but it is their impact on the major pests that usually attracts attention. However, when minor pests become important because of imbalances caused by the overuse of insecticides, disaster often follows (Reynolds et al. 1982).

Dynamics in Short Term Crops

Typically annual or short-term crops in temperate zones begin with soil preparation in late autumn and early spring, fertilization, preplant or preemergence applications of herbicides, planting, cultivation and harvest. In subtropical regions double or even multiple cropping may be possible within the yearly cycle. Rainfall distribution and temperature usually determine optimal planting dates and the length of the growing cycle. In cold high latitudes, soybeans must complete the cycle from planting to harvest in about 90 days. In the subtropics, the use of 140-day varieties is not uncommon (Hinson & Hartwig 1982). Throughout this cycle, soybean plants accrue biomass at an exponential rate and undergo profound physiological changes. The total above ground accumulation of biomass may reach 10 tons of dry matter per ha., partitioned throughout the season into vegetative and reproductive structures. As the cycle progresses, it is accompanied by a parallel increase in architectural and microclimatic complexity within the crop canopy and the underground structures that leads to the diversity and proliferation of potential feeding niches or food resources for colonizing herbivores. The availability of these resources is probably the most important single factor in setting numerical limits on species packing in a given community.

Kogan (1981) summarized the dynamics of variation of food resources in a typical annual field crop based on a soybean model. The exclusively crop-dependent components of a herbvivore's feeding niche have functional, spatial and temporal characteristics. Functional characteristics are determined by the physiology of the plant and refer to the various plant organs and tissues used differentially by various species of herbivores. Spatial characteristics depend on the stratification of the aerial and subterranean volumes of the plant and on the patterns of plants within fields. Such stratification may cause nutritional variability within and among plants (Denno & McClure 1985) or subtle but critical variability in microclimate closely related to an insect's ecological preferenda. Both functional and spatial characteristics vary in time, thus resulting in profound differences in plant resources at various phenological stages of development. The general pattern of the yearly ecological dynamics of a short term crop is an initial more or less long phase of gradual geometric increase in niche complexity and resource diversity open to herbivore occupancy, followed by a sudden drop in diversity and complexity as plants senesce and the crop reaches harvest maturity. This generalized pattern of crop dynamics presents a scenario of changing opportunities to potential herbivore colonizers and their complement of natural enemies. The instability of tritrophic interactions under these conditions is one of the major obstacles to classical biological control in short term crops.

Colonization of Short term Crops by Herbivores & Natural Enemies.--Colonization occurs both by herbivores and their natural enemies. The sources of colonizing species are varied and according to the crop may include the agroecosystem encompassing the crop (either a monoculture or a multiple crop system) and the relative geographic location of interacting agroecosystems. The first source of colonizers are well-adapted, host-specific, native species that overwinter in or near the crop field. Corn rootworms, Diabrotica spp., overwinter as eggs and colonize corn plants when the crop is grown without rotation with nonhost crops (Krysan et al. 1987). In temperate zones the harsh winters usually have a modulating effect on the survival of overwintering native species and thus affect the size of colonizing populations. In the midwestern United States, the bean leaf beetle, Cerotoma trifurcata Forster, and the Mexican bean beetle, Epilachna varivestis Mulsant, overwinter as adults in woodlots surrounding grain legume crop fields. The success of colonization usually depends on the synchronization of the emergence of the overwintered populations with the establishment of a host crop in fields adjacent to hibernacula. When spring planting is delayed because of insufficient or excess precipitation, the beetles may lack food or oviposition sites, and colonization may fail. These species usually remain on the crop, however, increasing gradually in succeeding generations if environmental conditions are favorable.

A second source of colonizers is polyphagous species, the populations of which increase on wild plants or on temporarily more attractive crops. These species migrate into a succession of crops as plants reach a preferred stage of growth or as the crops on which they had resided become unsuitable. The corn earworm, Heliothis zea (Boddie) develops on corn early in the season in North Carolina and produces two generations. When second generation adults emerge, the corn is no longer suitable and the moths disperse to such other crops as cotton, peanuts, and tomatoes and late planted soybeans at bloom. Waves of ovipositing moths often massive and generate damaging larval populations (Stinner et al. 1977, Kennedy & Margolies 1985). Also in this category are multivoltine species that arrive in small numbers onto a crop at various times during the season and may or may not become established. If they do their short life cycle and high reproductive rate result in the build up of populations that may prove damaging (e.g., aphids, whiteflies, leafhoppers and spider mites).

A third group of colonizers are migrant species that overwinter and reproduce early in the season in regions of subtropical climates. Successive generations expand their geographic range from the overwintering areas, generally following jet stream paths and the availability of suitable hosts (Sparks 1979, Rabb & Kennedy 1979).

An island biogeographical or dynamic equilibrium theory has been proposed as a model for the colonization of annual crops by arthropods (Price 1976, Mayse & Price 1978, Price & Waldbauer 1982). However, it has proven of small value in explaining or predicting patterns of colonization of short-term crops and its application has been criticized on both theoretical and practical grounds (Rey & McCoy 1979, Liss et al. 1986, Simberloff 1986). Although detailed studies on the dynamics of crop colonization under diverse cropping conditions ar few, those that exist suggest that the number of colonizing species increases as the crop matures and that a lag occurs between crop colonization by herbivores and subsequent colonization by natural enemies (Price 1976, Mayse & Price 1978).

It is important in the regulation of herbivore populations for natural enemies to follow herbivore colonizers closely. The availability of prey at an early stage of plant growth may determine the abundance of predators at later stages when other prey species may be present. Anecdotal accounts by soybean researchers in the southern United States (Harper et al. 1983) suggest that the green cloverworm, Plathypena scabra (F.) an early season herbivore, is a beneficial species because it serves as prey for the predaceous hemipterans. Later in the season those predators help moderate the population growth of such serious pest species as Heliothis zea, Anticarsia gemmatalis (Hübner), and Pseudoplusia includens Walker. The green cloverworm, however, is one of those migrant species that usually reach midwestern soybean fields at critical stages of crop development, and it therefore poses a potential threat in those areas.

Recruitment of Crop Colonizers.--The diversity of the arthropod community associated with annual crops seems to depend mainly on the extent of the area planted to that crop (Strong 1979). Plant architecture, however, influences the complexity of available feeding niches, and these ultimately determine the complexity and richness of those communities (Lawton 1978, Kogan 1981). Whether a crop is introduced or native is also important. Kogan (1981) considered three sources for species recruitment in introduced crops: (1) oligophagous species associated with native plants that have taxonomic or chemical affinity with the introduced crop, (2) polyphagous species capable of rapidly expanding their host range as new food resources become available or replace previous ones, and (3) oligophagous species that are associated with plants unrelated to the crop and that may undergo gradual host shifts. Native crops have a preponderance of host-specific, coevolved species and a full complement of effective natural enemies. The colonization of introduced hosts by native herbivores that originally fed on plant species closely related to the introduced crop has resulted in some of the most serious pest problems on record. The classic example is the Colorado potato beetle, Leptinotarsa decemlineata Say.

Short term crops are recolonized annually by a herbivorous fauna that varies spatially and temporally with the dynamics of the crop, the characteristics of the ecosystem, and the spatial relationship of the crop ecosystem to other adjacent or distant ecosystems. A complement of natural enemies associated with those herbivores usually colonizes the crop after a lag that is determined by the foraging patterns of the natural enemies and the sources of the colonizers. The build-up of natural populations of enemies depends on the availability of suitable prey or hosts. The nature and complexity of this colonizing arthropod fauna depend on whether the crop is native to or introduced into a region. Additionally, the colonizing fauna depends on how long the crop has been under cultivation, increasing exponentially for several growing cycles until it approaches a plateau determined by the area planted to the crop and the complexity of the crop's available feeding niches (Strong 1974, Lawton 1978, Kogan 1981). It is this rapidly changing and cyclically disturbed habitat that poses the greatest obstacles to the success of classical biological control in short term crops. Despite the inherent ecological instability of these crops, however, most herbivore populations are effectively regulated by a complement of natural enemies. This regulation is most dramatically demonstrated when natural enemies are inadvertently eliminated by broad-spectrum insecticides (Metcalf 1986).

Natural Control in Short term Crops

Short term crops in most growing regions of the world have a diverse and abundant population of natural control agents, especially if the fields have not been sterilized with broad spectrum pesticides.

Predators.--Many surveys have been conducted using as the target either the crop or particular species or guilds of species within a single crop or the various crops in a region. One of the most extensive surveys of natural enemies of any crop was conducted by Whitcomb & Bell (1964) in Arkansas cotton fields. There were 600 species of predators representing 45 families of insects, 19 families of spiders and 4 families of mites found. Other extensive surveys were done on spiders on soybean in other areas (Neal 1974, LeSar & Unzicker 1978). The number of unique species occurring at each location far exceeded the number of species occurring in common at any two locations combined or co-occurring at all locations. The spider community of cotton in Arkansas was far richer than the spider communities of soybean either in Florida or in Illinois. There were about as many species of spiders common to Arkansas cotton fields and Illinois soybean fields as there were to Arkansas cotton fields and Florida soybean fields, but there were three times more species in common in those two comparisons than there were species common to Florida and Illinois soybean fields. Although all three communities had a diverse spider population, the spider community of cotton was much more diverse.

Species composition was more influenced by geographic location than crop matrix. A similar comparison was made among surveys of carabids in Illinois and Iowa corn fields (Dritschilo & Erwin 1982), in North Carolina soybean fields (Deitz et al. 1976), and in Arkansas cotton fields (Whitcomb & Bell 1964). In contrast to the spider fauna, the carabids were much more localized. Only one species appeared in all three surveys, and only 18 species co-occurred in any two agroecosystems. Such comparisons suggest that crop communities have a rich fauna of predators and that many species are probably well adapted to local conditions. Although the effectiveness of this predaceous fauna has not been evaluated in detail, resurgences of pests are often attributed to the disruption of such natural control agents by broad spectrum pesticides (Shepard et al. 1977, Huffaker & Messenger 1976).

Parasitoids.--Assessments of naturally occurring parasitoids are usually based on surveys of individual host species or guilds of hosts. Extensive surveys have been conducted on the parasitoids of some of the major pests of short term crops (e.g., Heliothis zea, H. virescens, Nezara viridula). Heliothis zea and H. virescens have been recorded in the United States from 235 plant species in 36 families and are, therefore, highly polyphagous. A literature survey of the parasitoids of these two species produced 60 species of Hymenoptera in six families (Braconidae, Chalcididae, Eulophidae, Ichneumonidae, Scelionidae and Trichogrammatidae) and 62 species of Diptera in four families (Muscidae, Phoridae, Sarcophagidae and Tachinidae). The efficacy of natural control agents in cotton in North America was assessed by Goodenough et al. (1986).

A partial host record of N. viridula showed that it is also a highly polyphagous species, being recorded from 44 common cultivated and wild hosts in 18 different plant families (Todd & Herzog 1980). Jones (1988) surveyed the world literature for records of N. viridula parasitoids and found 57 species in two Diptera and in five Hymenoptera families.

Species guilds, rather than single species, are often the object of detailed studies. Comprehensive studies of parasitoids of lepidopterous caterpillars in soybean in the United States were reviewed by Pitre (1983). Ten primary parasitoids and 10 hyperparasitoids were recorded on cereal aphids in Europe (Vorley 1986). In most cases extensive surveys of common herbivorous insects of short term crops reveal the presence of a rich associated fauna of natural enemies. However, many of those herbivores remain serious pests. Obviously qualitative surveys reveal very little about the effectiveness of natural enemies in population regulation. The enrichment of the complement of natural enemies of short term crops through augmentive releases or through classical biological control offer means to counteract this situation.

Entomopathogens.--Entomopathogens are probably the most effective natural control agents in explosive pest populations in short term crops. A good example of the efficacy of a fungal pathogen in regulating lepidopterous caterpillar populations is the fungus Nomuraea rileyi (Farlow) Samson. This fungus is primarily a pathogen of many species of lepidopterous larvae (Ignoffo 1981). Natural epizootics frequently cause crashes of susceptible host populations. Under favorable environmental conditions this fungus may be the single most important mortality factor regulating populations of the velvetbean caterpillar, A. gemmatalis, in soybean fields in Brazil (Moscardi et al. 1984) and populations of the green cloverworm, P. scabra, in soybean in the midwestern United States (Pedigo et al. 1982). The success of the soybean IPM program in Brazil was due, to a great extent, to the correct assessment of natural epizootics of N. rileyi (Kogan et al. 1977, Kogan & Turnipseed 1987). However, epizootics are often not predictable and are occasionally too late in the growing season to prevent economic damage to the crop (Kish & Allen 1978, Ignoffo et al. 1975, 1981, Fuxa 1984). Despite these adverse characteristics of some epizootics, their dramatic natural has caused substantial research to be directed toward using N. rileyi as a biological control agent.

Heliothis zea and H. virescens on cotton in the United States are infected by many naturally occurring pathogens (Yearian et al 1986). The most common are: Nomurea rileyi and Entomophthora spp. fungi, Nosema heliothidis and Varimorpha necatrix, microsporidia, and the nuclear polyidrosis viruses of H. zea and Autographa california (Speyer). Although natural epizootics do occur, they are often inadequate to maintain Heliothis spp. populations below the economic injury level. Therefore, much effort has been directed to developing manipulative methods to enhance entomopathogen efficacy.

Classical Biological Control in Short term Crops

There are a few spectacular successes, which on examination again show that the success of a biological control program cannot be predicted on the basis of assumptions or preconceptions related to the ecological instability of the crop (Hokkanen 1985).

Southern Green Stink Bug--Nezara viridula (L.).--Southeast Asia is considered the center of origin of this species (Yukawa & Kiritani 1965). The pest is presently found throughout the tropics and subtropics of all continents. However, Hokkanen (1986) suggested that N. viridula is of Ethiopian origin, based on records of polymorphism as well as the number of host specific parasitoids in that region. Because it is an immigrant pest of many important crops, many attempts to establish parasitoids into newly invaded areas have been made. Programs in Hawaii and Australia have been very successful (Caltagirone 1981), and importation and release of natural enemies are currently being expanded in Africa, South America, New Zealand, Taiwan and the United States (Jones 1988). The success in Australia gives the greatest insight into the conditions for successful biological control of this insect.

Nezara viridula was first recorded in Australia in 1913 and has since been the subject of several successful biological control projects, mainly involving colonization of the egg parasitoid Trissolcus basalis imported from Egypt and Pakistan. The early history of control by importation of natural enemies was recorded by Clausen (1978), Caltagirone (1981) and Wilson (1960). Kogan et al. (1999) updated this history and assessed factors that may have led to the successful control of the pest in Australia.

The pest spread to the Ord Valley in northwestern Australia in 1974, over a decade after the last introduction of parasitoids from Pakistan to other parts of Australia. Within two years it had become a severe pest due to its polyphagous habit that enables it do damage many vegetable and field crops. Damage was so severe in sorghum that fields had to be abandoned. The parasitoid, T basalis was reared in an insectary and ca. 44,100 were released in fields in the Ord Valley. The host population began to decline due to parasitism a few months later and good control was obtained (Strickland 1981). Subsequent observations indicated that the parasitoids were usually present regardless of the level of abundance of the host population. Conditions that helped to maintain populations of stinkbugs at low levels and prevented their upsurge following their decline were explained by (1) the prevailing cropping system in the Ord Valley involved diverse plant species that were infested by the stink bug at different population levels. The parasitoids, therefore, were able to move from centers of high host population to centers of low host populations, thereby maintaining an overall low equilibrium position throughout the entire spectrum of crops; and (2) in addition to N. viridula, T. basalis attacked several other locally occurring pentatomids and thus had a continuous supply of hosts (Strickland 1981).

The success of T. basalis as the parasitoid of very mobile and polyphagous pest is attributable to a combination of the characteristics of its own host range and the characteristics of the feeding range of its host species. That combination guaranteed an environment that continually provided fresh adult parasitoids capable of keeping the pest a low population levels. As N. viridula is a major pest of many short term crops in most parts of the world, efforts to control it by means of natural enemies continue. According to Jones (1988), African and Asian egg parasitoids in the genera Trissolcus, Telenomus, and Gryon and six New World tachinid adult parasitoids deserve consideration in biological control. The tachinids are Trichopoda pennipes (F.), T. pilipes (F.), T. giacomellii (Blanchard), T. gustavoi (Mallea), Eutrichopodopis nitens Blanchard, and Ectophasiopis arcuata (Bigot).

Melon Fly Dacus cucurbitae Coquillet.--Native to the Indo-Malayan region, the melon fly was first recorded in Hawaii in 1897. Prior to its invasion, cucurbit crops were widely grown for local consumption and some were exported to California. Following the introduction of the fly, growing cantaloupes became impractical and the production of other melons, cucumbers and tomatoes was seriously curtailed (Nishida & Bess 1950). Biological control of the melon fly was undertaken by introducing Biosteres fletcheri (Silv.) from India. The parasitoids were mass reared in Hawaii, and field releases made in 1916 and 1917 resulted in their establishment. Two additional species Biosteres longicaudatus watersi Full. from India and B. angeleti Full. from Borneo, were introduced during 1950 and 1951, respectively (Clausen 1978). The 1916 and 1917 releases resulted in a 50% reduction of the melon fly populations, and although the flies were still a pest, melons were again a profitable crop in Hawaii (Fullaway 1920). Later the melon fly again became a severe pest requiring multiple applications of insecticides and generating additional control related research (Nishida & Bess 1950). Studies showed that the change in parasitoid efficiency was probably associated with changes in land use and agricultural practices (Newell et al. 1952, Nishida 1955).

Because melons and other perishable crops are available in the field for only a short period, these plants form an unstable resource to which the biology and life cycle of D. cucurbitae are well adapted. Consequently, parasitoids of the fly must be able to follow the short-lived and localized fly populations throughout their range if efficient control is to be achieved. In Hawaii, control had been possible because the presence of Momordica balsamina, the fruits of which constituted a stable wild host for D. cucurbitae and its parasitoids. Changes in agricultural practices and increased land use, however, reduced the areas where M. balsamina grew abundantly, thereby reducing the reservoirs of the natural enemies and making it more difficult for the natural enemies to reach the cultivated fields. The main fly population now had its origin in culti9vated fruits where parasitization was much lower than in the fruits of M. balsamina: 1% for tomatoes, 0-16.5% for melons, and 0.2-6.5% for cucumbers vs. 20-37.8% for M. balsamina (Nishida 1955). Thus, a change in the diversity of the habitat proved detrimental to this biological control project.

Cereal Leaf Beetle--Oulema melanoplus (L.).--A native pest of cereals in Europe, cereal leaf beetle was first recorded from Berien County, Michigan in 1962. According to Haynes & Gage (1981), damaging populations in the area were probably present since the 1940's. Expansion of the area infested by the cereal leaf beetle occurred rapidly and the current range extends through much of the Midwestern states to the East Coast. Strict interstage quarantines and treatment of potentially infested bales of hay and grain were enforced. Eradication efforts continued for about seven years, but were finally abandoned when the spread of the beetle obviously could not be halted. Probably widespread public opposition to the spray program influenced this decision.

The cereal leaf beetle has one generation per year and overwinters as unmated adults (Castro et al. 1965). With the spread of the beetle out of control, research was initiated in several areas, including sterile male techniques, behavioral control by means of attractants and biological control by means of imported natural enemies. Clausen (1978) summarized the biological control program. Initiated in 1963, the search for natural enemies concentrated in France, Italy and Germany. From 1964 to 1967 five parasitoids were imported and four to become established were Tetrastichus julis (Walk.), Diaparis carinifer (Thomsen), Lemophagus curtus Tow. and Anaphes flavipes (Foerster) (Haynes & Gage 1981).

Mass releases of A. flavipes were conducted in the absence of more efficient natural enemies. Releases were made in Indiana in 1966 and the parasitoid was recovered at most sites later in the same season. As the beetle was not easily reared in the laboratory, cultures of the parasitoid were maintained on beetles collected in the field. These beetles were also used in the screening of wheat, oats, and barley lines and varieties for resistance against the beetle. A parasitoid nursery was established in Niles, Michigan for the redistribution of parasitoids reared on field-infested populations.

Populations were observed to decline since 1971, with causes for the decline being attributed to a combination of such factors as weather-related mortality, mortality due to introduced parasitoids, genetic changes in beetle populations and changes in overwintering habitat (Haynes & Gage 1981). Although sporadic outbreaks may require treatment, populations of the beetle seem to have generally abated. This history suggests that immigrant pests, after an initial period of explosive expansion, may follow a pattern of adaptation within the agroecosystem that results in an equilibrium state not as detrimental to the crop.

Alfalfa Weevil--Hypera postica (Gyllenhal).--First found in the United States near Salt Lake City, Utah in 1904, Hypera postica is believed to have invaded from Europe (Titus 1907, 1910). The weevil was confined to 12 western states until 1952 when it was detected in Maryland (Bissell 1952). From Maryland it spread rapidly and is now found throughout North America.

There is one generation per year and winter is spent as aestivating adults and as eggs. Eggs hatch in spring about the time that alfalfa begins to grow. In the Midwest, larval feeding continues through May when pupation occurs. After emergence adults leave the field for available cover where they undergo summer aestivation. In autumn adults return to the field and begin laying eggs (Manglitz & App 1957).

Parasitoids were first introduced from Europe into the United States in 1911, and by 1919 they were well established in many areas of the western United States (Chamberlin 1924). Bathyplectes curculionis (Thomson) is the most widely distributed and most successful introduced parasitoid in the Midwestern U. S. During the 1960's and 1970's, both B. curculionis and B. anurus (Thomson) were released in Illinois by USDA personnel and are now found in most midwestern populations of the weevil (Dysart & Day 1976).

A fungal disease of alfalfa weevil larvae was found in Ontario, Canada in 1973 (Harcourt et al,. 1974), and was similar to that reported active on cloverleaf weevil, Hypera punctata (Arthur) by Arthur (1886). The fungus is believed to be Erynia phytonomi (Thomson) and actually differs from that attacking cloverleaf weevil. It was found to spread rapidly out of Ontario to other portions of North America (Muka 1976, Puttler et al. 1978, Barney et al 1980, Los & Allen 1983, Nordin et al. 1983). It is now considered to be the major naturally occurring biological control agent of the alfalfa weevil throughout most of its range (Carruthers & Soper 1987). A similar fungus causes comparable mortality in Hypera variabilis in Israel (Ben Ze'ev & Kenneth 1982).

Erynia phytonomi overwinters in the soil as thick-walled resting spores that germinate in springtime to produce germ conidia, which infect weevil larvae. Conidia produced by infected larvae are responsible for the horizontal transmission of the disease (Ben Ze'ev & Kenneth 1982). Younger larvae tend to produce conidia and older larvae resting spores (Watson et al. 1980). Brown & Nordin (1982) developed a detailed model of this disease and estimated that the first incidence occurs in Kentucky after an accumulation of 220 to 290 degree days. Then the alfalfa weevil population has to reach a threshold density in order to allow for sufficient horizontal transmission for an epizootic. Brown & Nordin (1982) estimated this threshold to be 1.7 weevil larvae per stem. Mortality rates caused by the fungus are often quite high (30-70%) at the time of peak larval occurrence and often 100% later in the season (Morris 1985). It is restricted in effectiveness as a biological control agent because it often appears late relative to currently recommended harvest dates (Armbrust et al. 1985). Brown & Nordin (1982) proposed using computer-directed harvest dates that are earlier than normally recommended. The microenvironment in windrows promotes an earlier than normal epizootic and reduces the need for insecticides.

The appearance of the fungus as a major mortality factor after the two above mentioned parasitoids were established poses the question of how these all will now coexist, especially as they attack the larval stage. About five days elapse from infection to death in diseased larvae and parasitized larvae die within 10 days. Such time periods suggest that an alfalfa weevil larva infected and parasitized simultaneously would probably die from the fungus before the parasitoid completed its development. Field studies indicate that the disease has a negative impact on the two parasitoids (Los & Allen 1983, Loan 1981, Morris 1985).

European Corn Borer--Ostrinia nubilalis (Hübner).--This insect is believed to have been accidentally introduced in shipments of broom corn from Europe in the area of Boston, Massachusetts in 1917 (Caffrey & Worthley 1927). Its range presently includes most of the major corn producing regions of the United States. Between 1920-1930 24 species of parasitoids were imported into the United States from Europe and the Orient, and by 1962 six of these were established. Two of the introduced parasitoids, the tachinid Lydella thompsoni (Herting) and the ichneumonid Eriborus terebrons (Gravenhorst), usually parasitizes up to 50 percent of the borers in the Midwest during 1958-1963. However, in the 1960's parasitism by the tachinid decreased rapidly and few, if any , can now be found in the United States (Hill et al. 1978, Burbutis et al. 1981).

Explanations to explain the decline of the tachinid center around competition from the microsporidian Nosema pyrausta. Presently the only parasitoid commonly found in the Midwest is the braconid Macrocentrus grandii (Goidanich), which is infected by N. pyrausta and high levels of mortality result (Andreadis 1980, 1982; Siegel et al. 1986). In Illinois in 1982 and 1983, M. grandii parasitized an average of 19.5% of first generation corn borer larvae, but only an average of 5% of second generation larvae . This is believed due to the fact that first generation borer populations usually have a lower prevalence of Nosema than second generation populations, and thus the parasitoid may avoid the disease by parasitizing primarily first generation larvae.

Paillot (1927) first described N. pyrausta from European corn borers collected in France, and the pathogen was first found by Steinhaus (1951) in the United States in larval European corn borers from the Midwest. It now infects corn borers throughout most of their range, and a high prevalence (up to 100%) have been reported from many states (Van Denburg & Burbutis 1962, Hill & Gary 1979, Andreadis 1984, Siegel et al. 1987). This microsporidian infects most body tissues, and infectious spores are passed in the feces of infected larvae. Horizontal transmission occurs when healthy larvae ingest sufficient numbers of spores, usually in larval tunnels contaminated by frass from infected larvae. Although some disease-induced mortality occurs when larvae are infected by oral ingestion of spores, the most dramatic mortality occurs when transmission is transovarial (Windels et al. 1976). Such larvae experience 30-80 percent higher mortality than healthy larvae (Kramer 1959, Windels et al. 1976, Siegel et al. 1987). Crashes usually occur after several years of rising corn borer populations and when the prevalence of Nosema nears 100 percent. Because horizontal transmission of infection in corn borer populations depends on the probability of healthy larvae inhabiting a corn stalk with infected larvae, the initial infection level of transovarially (vertical infection) infected larvae and the larval population density are two of the most important variables affecting infection levels in corn borer populations (Maddox 1987).

Although in many areas of the United States N. pyrausta is the most important biological mortality factor in corn borer populations, it has little promise as a microbial insecticide because it is already widely distributed. During some years the fungus Beauveria bassiana causes considerable larval mortality in central Iowa and west central Illinois by Marcos Kogan and associates.

Cassava Mealybug in Africa--Phenacoccus manihoti Matile-Ferrero.--A major food source for over 300 million people in tropical regions of the world, cassava is an important root crop (Bellotti & Schoonhoven 1985). Most production (80%) is concentrated in Brazil, Indonesia, Nigeria, Zaire, India and Thailand. This plant is native to tropical South America, and was introduced to the Congo basin in Africa in the early 16th Century (Cock 1985). Although a perennial shrub reproducing vegetatively, cassava roots may be harvested 7 to 18 months after planting. Roots are harvested by pulling the stems and uprooting the whole plant.

Mealybugs of the genus Phenacoccus have been recorded in association with cassava in South America and Africa. Penaacoccus gossypii Towns. & Cock, P. grenadensis Green & Laing, and P. madeirensis Green are polyphagous, but P manihoti Matile-Ferrero appears specific to cassava and the only species capable of producing severe distortion of leaves. Another South American species was separated from P. manihoti and described as P. Herreni Cox & Williams (Cox & Williams 1981). Mealybug damage seems to be a recent phenomenon, but one that is increasing in areas where it had not previously been found (Bellotti et al. 1985). This new pest status results from an imbalance between the mealybug, the local cassava land race and the existing natural enemies. The situation was particularly acute in Africa. Phenacoccus manihoti was first discovered in Zaire in 1973 and spread into almost all other cassava growing areas of the continent. The estimated losses caused by this species and another explosive pest, cassava green spider mites, Mononychellus spp., were estimated at $2.0 billion per year, and the pests affected an area about 5.5 million ha. (Neuschwander et al. 1984).

Control of the mealybug with natural enemies was attempted following its recognition as an immigrant species (Cox & Williams 1981). Surveys for native natural enemies associated with P. manihoti in Gabon revealed that various guilds have incorporated the immigrant in their host or prey range, but none were greatly efficient (Boussienguet 1986). The list included two primary parasitoids, four hyperparasitoids, nine predators and eight parasitoids of the predatory species (Neuenschwander et al. 1987). Extensive explorations for natural enemies were conducted in South America. Between 1977 and 1981 the Commonwealth Institute of Biological Control in collaboration with the International Institute For Tropical Agriculture surveyed the tropical areas of central and northern South America and found that the parasitoids Aenasius vexans Kerrich, Apoanagyrus diversicornis (Howard), and Anagyrus spp. seemed to be specific to the cassava mealybug (Cox & Williams 1981). In 1980 a species of Diomus (Coccinellidae) was imported and released in experimental fields (IITA 1981, 1985), and one year later the encyrtid Epidinocarsis lopezi (DeSantis), collected in Paraguay by M. Yaseen, was imported to Nigeria and released at two sites. The parasitoids were established and recovered from parasitized mealybugs. (Lema & Herren 1985).

The spread of E. lopezi was spectacular; by December of 1985 it had become established over 650,.000 km² in 13 African countries (Neuenschwander et al. 1987). Exclusion experiments and continuous monitoring demonstrated the efficiency of the parasitoid in regulating P. manihoti populations in Africa. IITA (1985) reported that a significant reduction in population levels of the cassava mealybug had been observed in all regions colonized by E. lopezi. In those areas, the mealybug was recorded at populations of 10-20 per terminal cassava shoot. Prior to the establishment of the parasitoid peak populations in excess of 1,500 per shoot were common (IITA 1985). The successful importation and establishment of E. lopezi gave further impetus to the biological control program at IITA, and additional species of parasitoids and predators are being released experimentally with various degrees of success (IITA 1987b).

Detailed biological studies have been conducted on the coccinellid Hyperaspis raynevali Mulsant (Kiyindou & Fabres 1987), and the entomophthoraceous fungus Neozygites fumosa (Speare) Remaudiere & Keller (Le Ru 1986). This successful biological control program of cassava mealybug in Africa is probably one of the best demonstrations of the potential of this tactic for IPM in short term crops. However, other tactics are being used against this and other cassava pests, including breeding of plant resistance, cultural control and the selective use of pesticides (Cock & Reyes 1985).

Other Systems (e.g., cotton).--Please consult the case history series (CH-..) and the references for details on pink and spotted bollworms in cotton. [ Please refer also to Related Research ]

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