All insects and plants, to various degrees, are attacked by natural enemies independent of any deliberate manipulations by people. Such natural control is rarely sufficient to suppress an invasive species: the local natural enemies lack specialized relationships to the invader, since by definition, the new pest is outside the evolutionary experience of the prey species. For native species, however, natural control may suppress plants and insects below pest levels. Also, for invasive species against which specialized natural enemies have been imported and established, the latter become part of the fauna, providing naturally occurring control. Thus, for all species, apart from invaders not yet subject to natural enemy importations, natural control exists and may be sufficient to suppress such pests adequately for human needs. However, in crops and other artificial landscapes, people can disrupt natural control, particularly with the application of pesticides that kill, sterilize, or repel important natural enemies. Conservation as a form of biological control aims to avoid this loss of natural control either from the use of pesticides or habitat simplification. Sometimes active intervention on behalf of natural enemies to provide them with key missing foods or hosts is necessary.
Before 1947, few synthetic pesticides were used in crops. Most available materials were stomach poisons based on heavy metals such as lead and arsenic, which kill only if eaten. Some botanical extracts, such as rotenone and pyrethrum, both of which quickly degrade in the environment, were also used. After World War II, a business revolution occurred when it became recognized that a variety of compounds that could be artificially synthesized in laboratories were highly effective in killing insects by mere physical contact. Beginning with DDT in 1947, many types of chemicals were marketed to kill insects. One of the undesirable consequences of this change in farming practice was the mass destruction of beneficial insects in crops, resulting in a substantial decrease in natural control. Indeed, insecticides often killed natural enemies more efficiently than they killed the target pest. This unintended consequence was due to the smaller body size, greater relative surface area, and lower levels of detoxification enzymes possessed by parasitic Hymenoptera and other natural enemies, compared with herbivorous pests.
pest resurgence Occasionally, farmers found that pests for which they applied pesticides were, within a few months, more numerous than they had been before the application of insecticide. This population rebound has been termed pest resurgence. The steps in resurgence are as follows:
1. The pest population is reduced by the insecticide.
2. The same insecticide application destroys most of the natural enemies that were partially suppressing the pest before the application.
3. Natural enemies are slower to increase in number than the pest after the pesticide residue from the application has degraded to levels unable to kill insects.
4. In the absence of the pesticide and with few remaining natural enemies, the survival and reproductive rates of the pest population increase, leading to higher densities.
In rice crops in Asia, outbreaks of a sucking insect called rice brown planthopper (Nilaparvata lugens) were rare before the 1960s. In the 1970s, outbreaks occurred with greater frequency and intensity, as insecticide use increased to control this pest. Research conducted at the International Rice Research Institute in the Philippines demonstrated that this was a classic example of pest resurgence and that pesticide applications were destroying spiders and other generalist predators that were otherwise usually able to suppress rice brown planthopper. As farmers used pesticides more often, outbreaks became larger and more frequent. This phenomenon led to a pesticide treadmill for rice brown planthopper control. A program of grower education was supported by the Food and Agriculture Organization of the United Nations to help rice farmers to understand pest resurgence, natural enemy recognition, and the beneficial role of natural enemies in rice paddies. This outreach program successfully reduced pesticide use on rice crops in Asia, ending a cycle of damaging pesticide use and crop loss.
secondary pest outbreak A related population process occurs when insecticides applied to suppress a primary pest induce a different species, formerly not damaging, to become a pest. This is called a secondary pest outbreak. In apple crops in the eastern United States, growers must control two serious direct pests of the fruit, apple maggot (Rhagoletis pomonella) and plum curculio (Conotrachelus nenuphar). These species are most often controlled by repeated application of insecticides to foliage with chemicals that have long periods of residual activity. These applications destroy the parasitoids of leafminers and predators associated with spider mites. Outbreaks of these two foliar pests later in the summer are a direct consequence of grower efforts to control these two key fruit pests.
seeking pesticides compatible with natural enemies To reduce the destruction of natural enemy populations caused by insecticides, there are two potential solutions: using pesticides that have intrinsically selective action or using application systems that are ecologically selective.
Selective Pesticides Three kinds of insecticide have shown the greatest compatibility with natural enemies: stomach poisons, systemic pesticides, and insect growth regulators. Stomach poisons are materials that must be ingested to kill. Materials such as the microbial pesticide. B. thuringiensis and some mineral compounds such as kryolite are examples. Pests eating foliage with residues of these materials are killed, but natural enemies walking on treated foliage are not affected.
Systemic pesticides are materials that enter plant tissues and are translocated through the plant. These compounds may be applied to soil and absorbed by roots, or they may move translaminarly into leaves after application to the foliage. Because residues are available only to insects that feed on the crops' tissue or sap, natural enemies resting or walking on plants are not affected.
Insect growth regulators are chemicals that mimic or disrupt insect hormones, preventing normal molting. These compounds kill only when the insect tries to molt. Such materials can be selective if only the pest is likely to be exposed in a susceptible stage. In principle, screening programs could identify specific insecticide—natural enemy combinations in which any contact pesticide might turn out to be selective relative to some particular natural enemy. However, because such materials tend to be rare and screening trials to discover them are costly, only a few are available.
Ecologically Selective Methods of Pesticide Use Manipulation of a pesticide's formulation, timing, or method of application is another method for achieving selectivity in control. Granular formulations of pesticides that fall to the soil, for example, are unlikely to damage natural enemies that forage for hosts or prey on the foliage. Thus, a granular material may be applied at transplant into a cabbage field to protect the roots of young plants from feeding in the soil by larvae of cabbage maggot (Delia radicum) without injuring the braconid parasitoids that search the leaves to find and parasitize cabbage aphids (Brevicoryne brassicae). More complex methods of separating the pesticide from the natural enemies exist, such as monitoring the emergence of key natural enemies and applying pesticides either earlier or later than the peak activity period of the natural enemy. However, methods that require effort on the part of growers, or are at all complex, tend not to be used.
Loss of Natural Control through Simplification of Crop Fields
Natural control of pest insects and mites in crops has also been reduced by habitat simplification and physical changes in crop plants used in commercial, large-scale agriculture. To sustain their populations, parasitoids need hosts, carbohydrates, and secure places to live that are not subject to insecticide application or physical destruction by plowing, flooding, or fire. Predators need prey and can benefit from or even subsist on alternative nonprey foods such as pollen.
Natural control in crops can be maintained or improved by considering the degree to which these basic necessities of natural enemies are provided within or adjacent to the crop. A few examples illustrate the process.
adding pollen to enhance predator mites
Phytoseiid predatory mites are often important in control of pest spider mites. In some crops, numbers of such phytoseiids may be too low to provide effective control. One approach to increasing phytoseiid numbers is to provide pollen as an alternative food, especially for periods when spider mite densities are low. Levels of pollen on foliage of citrus and other orchard crops may be increased by use of species of trees in windbreaks around orchards or species of grasses as ground covers within orchards that are prolific pollen producers. Effective use of this approach has been made in South African citrus orchards for control of citrus thrips (Scirtothrips aurantii) with the phytoseiid Euseius addoensis addoensis.
keeping useful structures on plants Many plants, such as cotton, have sugar-secreting glands called nectaries both inside and outside of flowers. Many species of natural enemies feed on these sugars. Plant breeding has made it possible to eliminate such nectaries in some crops, and this is sometimes done to deny pests access to the carbohydrate resources. The decision to eliminate or retain necataries needs to be based on studies of the net benefit to pest control of these structures. Plants (e.g., grapes) also often have on their leaves pits or pockets, called domatia, that provide physical refuges for phytoseiid mites. Varieties with domatia often have higher phytoseiid densities and fewer pest mites. Retention of such structures in new crop varieties may be important and should be an explicit part of plant breeding.
enhancing spaces between crop rows or around crop fields as refuges Natural enemies of some species remain tightly linked to the plant and are little affected by the larger environment. Parasitoids of scales on citrus trees, for example, have all their needs met on citrus trees, provided insecticides are not used and some scales are present year-round for parasitism, host feeding (feeding on host body fluids), or production of honeydew (a sticky carbohydrate waste product produced by homopterans that parasitoids use for food). Other species of natural enemies move about more, passing through the spaces between crops rows, or moving back and forth between crops and noncrop vegetation in uncultivated borders. Species such as spiders and carabid beetles are generalist predators of value in vegetable plantings. However, bare or plowed soil between rows often becomes too dry and hot to favor these predators. Reduced tillage, through greater use of herbicides, or use of cover crops between rows, can enhance populations of these predators. Plants between crop rows, however, must not compete with the cash crop for water or nutrients, or crop yield may be reduced. In cereal crops in the United Kingdom, populations of ground beetles, generalist predators that eat cereal aphids, can be increased by leaving low dikes through fields that are not plowed. These dikes produce perennial grass and herb communities that act as refuges for carabid beetles, which then forage in the cereal plots and consume aphids. Also, in crops that are sometimes treated with pesticides, nontreated patches of noncrop vegetation along crop borders can act to reinoculate crops with natural enemies.
Extent of Successful Use of Natural Enemy Conservation
Natural control is ubiquitous and contributes extensively to pest control in most settings. Conservation of natural enemies through reduction of conflicts with pesticides is a major focus of integrated pest management (IPM) philosophy and practice, and many studies have been conducted that have led to better conservation of natural enemies in crops such as citrus, avocados, apples, and greenhouse tomatoes. Because it is often associated with reductions in out-of-pocket costs, this form of conservation is particularly acceptable to growers, who often are asked to reduce or stop altogether a costly practice (such as applying a pesticide). In contrast, practices that require positive action, such as providing a resource or manipulating vegetation in or near the crop, have been adopted much less often. To be valued by growers, such measures must clearly produce pest control benefits that significantly exceed the costs of undertaking them. Practical use of these ideas presently is limited to organic growers and others who wish to produce crops with little or no use of synthetic pesticides.
Conservation biological control is universally considered to be a very safe activity. Measures to reduce insecticide use, or to convert to selective or compatible materials, both reduce risks to people working on or living near farms and minimize environmental contamination.
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