Biological Control Through Augmentation

Pros and Cons of Augmenting Natural Enemies

Entomologists and farmers, working together, have developed methods to rear some species of predators and parasitoids that attack pest insects. This approach of deliberately rearing natural enemies and releasing them against target pests has been applied against insects and mites of both greenhouse and outdoor crops.

The use of this practice in greenhouse-grown tomatoes was begun in the 1920s with the rearing by English growers of Encarsia formosa, a parasitoid of the greenhouse whitefly

(Trialeurodes vaporariorum). This control program died out because of grower use of pesticides. Biological control was revived in the 1970s by Dutch greenhouse tomato growers because whiteflies had developed resistance to pesticides. In greenhouses that are closed up against the cold early in the crop cycle, natural enemies may be scarce or absent. Augmentative biological control was seen as a way of correcting this natural enemy absence. Natural enemy rearing for the greenhouse industry started when one grower began producing natural enemies for his own use, but soon he was selling surplus parasitoids or predators to other growers, and the operation became a separate business (an insectary). From 1970 to 2000, the number of commercial insectaries grew from just a few to several dozen firms, which collectively produce about 100 species of natural enemies for sale. A few species (mainly the parasitoid E. formosa and the predatory mite Phytoseiulus persimilis), however, make up most of the sales. Today, a variety of natural enemies are used in indoor settings that include greenhouses, plant conservatories, mushroom houses, and animal holding buildings such as dairies, hog-rearing facilities, poultry barns, and zoos.

Outdoor releases of several species of predators and para-sitoids are regularly made by growers in various countries. Egg parasitoids in the genus Trichogramma (Hymenoptera: Trichogrammatidae) have been used extensively throughout the twentieth century to suppress pest weevils and caterpillars in cotton, corn, and sugarcane, especially in China, Russia, and tropical sugar-producing countries. Predators of mealybugs for release on citrus crops in parts of California have been reared by a growers' cooperative since 1926. One of the more common current uses of augmentative biological control on outdoor crops is the release of various species of predatory phytoseiid mites for control of pest spider mites, an approach that has been used most often with strawberries and with foliage plants grown outdoors in shade houses.

There are two different approaches to augmentative biological control. Most indoor releases of natural enemies intend only to seed the crop with a founding population of the natural enemy, which then reproduces and eventually suppresses the pest after its numbers have increased naturally in the crop. This approach is called inoculative biological control. Cost of this approach is minimized because smaller numbers of the natural enemy are needed. In contrast, with inundative biological control, an attempt is made to release enough natural enemies to control the pest immediately. Because much higher numbers are released, this approach is economical only against natural enemies with very low production costs, and use has been most successful on crops with a high cash value per hectare.

How Insectaries Turn Natural Enemies into Mass Market Products

To profitably market a natural enemy, an insectary must succeed in a series of activities.

1. Find a suitable natural enemy. Commercial augmentative biological control starts with the discovery of a natural enemy that research suggests may be effective. The natural enemy must attack an important pest efficiently, be able to be reared under mass production conditions, be easily harvested and able to survive transit stress, and be competitive in price with other forms of pest control available to growers.

2. Develop a mass rearing system. To commercially produce a natural enemy, insectaries must be able to make a financial profit on the species. Successful production systems vary. For some species, such as whitefly parasitoids, production can use natural hosts on their favored plants. E. formosa, for example, is reared in greenhouse whitefly produced on tobacco plants. Similarly, the important predatory mite. P. persimilis is grown on the spider mite Tetranychus pacificus on bean plants in greenhouses. In other examples, costs of production or the scale of production are improved by rearing species other than the target pest. Most Trichogramma wasp species are grown on the eggs of moths that feed on stored grain, rather than on eggs of the target moths themselves, because colonies of grain-feeding moths can be reared much more cheaply, allowing the production of Trichogramma in huge numbers at low cost.

3. Develop harvest, storage, and shipping methods to get the product to customers. Most predators and parasitoids must be used within a few days or weeks of production. For some species, induction of an arrested state called diapause can be used to store immature parasitoids inside parasitized hosts for months. Shipping to customers must use rapid transport (1—3 days) and avoid delays at international borders. Longer delays invariably result in the deaths of natural enemies due to heat, desiccation, continued development, or starvation.

4. Provide clear instructions on effective release methods and rates for customers. The final step in the effective use of natural enemies reared in insectaries is their release by the farmer at the right rate and in the correct manner. Effective rates are discovered by controlled trials in universities and government laboratories, and by ascertaining the experience of growers who have used products in accordance with advice from producers.

Extent of Successful Use indoor crops The use of augmentative biological control has become widespread in greenhouses in northern Europe and Canada that produce vegetables, with over 5000 ha using E. formosa for whitefly control and over 2800 ha using P. persimilis for spider mite control. These amounts, however, still represent only a small percentage of the world's protected culture because these biological control agents are used much less often in southern Europe and Japan, areas with extensive greenhouse vegetable production but with differences in temperatures and open rather than closed greenhouses. Similarly, use of biological control is very limited in greenhouses producing bedding plants or floral crops, the major focus of greenhouse production in the United States.

outdoor crops The scientific use of augmentative natural enemy releases in outdoor crops is best established in northern Europe for control of European corn borer (Ostrinia nubilalis) in corn. Use is greatest in Germany and France, where over 3200 ha is protected annually with Trichogramma releases. This fraction is, however, small compared with the total corn acreage in Europe, and use of biological control is concentrated principally where pesticide use is not allowed because of concern for health of people living near cornfields. Natural enemy releases for mite control have been successful in strawberries in California, Florida, and the northeastern United States, and in outdoor shade houses used for production of foliage plants in Florida. In Mexico, Russia, China, and other countries, large-scale releases of Trichogramma spp. have been made for a variety of moth and beetle pests of corn, sorghum, and cotton, but the efficacy of these releases has not been well demonstrated. Some of these activities have been state supported, and their actual economic value for pest control is not clear.

Safety

Release of parasitoids and predators replaces pesticide application and thus enhances human safety. For workers in insectaries, handling of large quantities of insects or mites constitutes an allergy risk. Where problems arise, risk can be reduced through air exchange or filtration to reduce concentrations of airborne particles and through use of gloves and long-sleeved shirts to reduce skin contact with arthropod body fragments. Risk to native species posed by releases of nonnative natural enemies can be of concern, as well. Generalist, nonnative species released in large numbers may establish outdoors and attack or suppress populations of native species, or they may reduce densities of native natural enemies through competition for resources. Consequently, some governments, such as those of Hawaii, Australia, and New Zealand, restrict importation of natural enemies used in augmentative biological control. For example, importation of North American green lacewing species (Neuroptera: Chrysopidae, Chrysopa spp.), used in greenhouses as predators of aphids, might lead to establishment of such species in the wild, increasing competition with the endemic native lacewings in Hawaii, which have conservation value as unique native wildlife.

MICROBIAL PESTICIDES Using Microbes as Tools

Insects suffer from diseases caused by pathogens of several kinds, including bacteria, viruses, fungi, nematodes, and protozoa. Sometimes natural outbreaks of disease occur that locally and temporarily influence the density of pest populations. Microbial control seeks to use pathogens as tools to suppress pest insects. This process involves finding pathogens able to kill pest species of concern, followed by development of methods to rear pathogens economically. Methods must be developed to store the pathogen's infective stages without loss of viability and to apply the pathogen to the target in ways that result in high rates of infection and thus control. Details of the biology of each pathogen and the effects of environmental conditions on infectivity after application are crucial in determining whether any given pathogen can be used effectively as a microbial pesticide.

Bacteria

Many of the bacteria that infect insects are lethal only in stressed insects because the bacteria, lacking effective means of escaping from the host's gut after ingestion, are unable to enter its body cavity. Species in the genera Bacillus (B. thuringiensis, B. sphaericus, and B. popililae) and Serratia (S. entomophila) are the main bacteria that have been used as microbial pesticides. Of these, only B. thuringiensis has been widely successful. This species produces toxic crystalline proteins inside its spores. Crystals from different strains of this bacterium vary in their ability to bind to the gut membranes of different species, thus shaping the host ranges of each subspecies of the pathogen. If crystals are able to bind to the gut membranes, these tissues are degraded, allowing bacteria to penetrate the body cavity and kill the host.

Strains discovered in the 1920s infected only some species of caterpillars. Later, new strains were discovered that were able to infect mosquito larvae, chrysomelid beetle larvae (such as the Colorado potato beetle, L. decemlineata), and scarabs (such as the Japanese beetle, Popillia japonica). Commercial use of this pathogen is possible because it can be successfully mass-reared in fermentation media without any use of living hosts. This makes its production inexpensive. Applications of B. thuringiensis have advantages for use in forests, where residues of conventional pesticides are objectionable because of potential harm to native wildlife, and in IPM programs in crops where conservation of natural enemies is desired. B. thuringiensis is compatible with most natural enemies because it must be ingested to have any effect and because its toxic proteins are selective in their gut binding properties. Genes from B. thuringiensis that code for toxic proteins have been isolated and inserted into plants where they are expressed and produce insecticidal proteins in plant tissue and pollen. Transgenic varieties of such major crops as corn, soybeans, and cotton exist and are widely planted in the United States.

Other species of bacteria have had limited commercial use. B. sphaericus is formulated for use against some species of mosquito larvae. B. popilliae was once commercially produced for use against larvae of Japanese beetle (an important pest of turf), but this bacterium must be reared in living host larvae, which has made its production uneconomical. In New Zealand, S. entomophila causes an infection known as amber disease in a native turf grub (Costelytra zealandica), and its commercial use is being promoted. As with B. thuringiensis, the ability of S. entomophila to be reared in fermentation media apart from living hosts has been a key feature in promoting its commercial use.

Fungi

Species of Deuteromycotina fungi in several genera, including Beauveria, Metarhizium, Verticillium, and Hirsutella, infect insects and can be grown on fermentation media in solid culture. The spores of these species, when applied, adhere to the bodies of insects, and special hyphae from the spores use enzymes and mechanical pressure to penetrate through the insect's cuticle to cause infection. Infection requires spore germination, a process that is sensitive to environmental conditions. In general, many fungal strains or species require a minimum number of hours (often 12—24) of high relative humidity (often above 80%) to germinate. However, these requirements vary within species and among isolates from different locations and hosts. Spore germination requirements, if not met, can lead to control failures. Successful commercial use of entomopathogenic fungi has focused on ways to either meet these requirements by manipulating the formulations of the product applied (e.g., adding oils when used in arid climates), using these products in inherently favorable climates (e.g., greenhouses), using them in favorable habitats (e.g., soil), or finding strains or species with less stringent environmental requirements for spore germination. Commercial use of these fungi is also affected, but not prevented, by the inability of most species of fungi to produce spores under water. This prevents the use of liquid culture methods, requiring the use of solid media (like boiled rice) or a diphasic system in which mycelial growth takes place in liquid culture, followed by plating out of fungi on solid media for spore production as a second production step.

Successful use of microbial pesticides based on fungi has been achieved by an international consortium (LUBILOSA) in Africa, which has developed the fungus Metarhizium anisopliae var. acridum (Green Muscle) for control of locusts in Africa. This locust control project is highly beneficial to the environment because this selective, naturally occurring fungus replaces the use of highly toxic, often persistent, pesticides such as dieldrin. Field trials in a number of African countries have demonstrated both high levels of efficacy and costs competitive with the use of conventional pesticides (about U.S. $12 ha-1). Success in this effort involved screening over 160 isolates of fungi to find the best fungus and the development of formulations for both storage (without refrigeration in hot climates) and application. Field trials demonstrated high initial levels of mortality and pathogen recycling, leading to persistence of suppression.

Similar success of fungal pesticides in general agriculture has not yet occurred. In the United States, for example, only one species, Beauveria bassiana, is commercially available, and its use is extremely limited.

Nematodes

Nematodes are multicellular organisms as opposed to unicellular microbes, but they are formulated and applied like microbial pesticides. Nematodes in more than 10 families infect insects, but only those in the families Steinernematidae and Heterorhabditidae have been commercially employed for insect control. These species, unlike those in other families, can be reared in fermentation media apart from living hosts. Techniques for large-scale production in liquid broths containing ingredients from dog food can be used to rear about six species in these families. Entomophagous nematodes actively penetrate insect hosts through the insect integument or natural body openings (spiracles, mouth, anus). Once inside the insect body cavity, the nematode defecates specialized bacteria that it carries symbiotically. These bacteria (in the genera Xenorhabdus and Photorhabdus) quickly kill the host with toxins. Nematodes then reproduce as saprophytes in the decaying host tissues. Entomopathogenic nematodes are sensitive to desiccation, which has limited their use in pest control. Applications made to dry foliage are ineffective because nematodes usually die before encountering hosts. Successful use of these nematodes has been limited to control of pests in moist habitats, such as fungus gnats and scarab grubs in soil, and lepidopteran borers in plant stems.

Viruses

Insects are subject to infections by viruses in a number of families. However, only those in the highly specialized Baculoviridae have been considered for use as microbial pesticides. Viruses in this family infect only insects and are very safe to people and wildlife. However, all viruses are obligate parasites of living cells, and none can be grown in fermentation media. Currently, they are produced in live host insects, which themselves must be mass-reared. This makes viral products relatively expensive, although the governments of some countries, notably Brazil, have promoted their use. A further aspect of the biology of viruses is their high level of host specificity. Extreme specificity of viruses reduces the economic value of products because they kill very few species of pests. Because of these economic factors, no virus products have been economically successful in the United States or Europe, although a few have been developed and briefly marketed.

Safety of Microbial Pesticides

In the United States and many other countries, microbial preparations (but not nematodes) sold for pest control are considered to be pesticides that require government approval and product registration before sale. Requirements for registration have been modified to reflect differences between chemical and microbial pesticides. Manufacturers are required to specify the exact identity of the microbe in their products, the production process, including controls to prevent contamination, and safety data on infection and allergenic properties of the pathogen and the product as a whole. The safety record to date suggests that risks from such products are either nonexistent or too low to detect.

Degree of Use

Except for genetically transformed plants that express the B. thuringiensis toxin (which are not microbial pesticides, but a related development), microbial pesticides are niche products. In no control programs have microbial pesticides widely displaced synthetic pesticides from pest control markets. B. thuringiensis is the most widely used organism, but B. thuringiensis products represent 1 to 2% of the pesticide market. These products do, however, have important value as pesticides because they are more readily incorporated into IPM programs that include natural enemies.

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