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Report of the Research Bneftug Panel on Biological Control in Managed Ecosystems

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Research Beefing Panel on Biological Control in Managed Ecosystems R. lames Cook (Chairman), Reseach Leader, Root Disease and Biological Control Research Unit, USDA-ARS- Washington State University, Pullman Lloyd Andres, Research Entomologist, USDA-ARS, Albany, Calif. Gustaaf A. de Zoeten, Professor of Plant Pathology, University of Wisconsin, Madison Charles Doane, Director of Research anct Development, Scentry, Inc., Buckeye, Ariz. l Robert W. Gwadz, Scientist Director, USPHS, and Head, Meclical Entomology Unit, NATD/N1[H, Bethesda, Md. Ralph W. F. Hardy, President, Boyce Thompson Institute for Plant Research, Ithaca, N.Y. Bruce Hemming, Research Specialist, Plant Microbiology, Monsanto Life Sciences Research Center, St. Louis, Mo. Joseph Kuc, Professor of Plant Microbiology, University of Kentucky, Lexington Reinhold Mankau, Professor of Nematology, University of California, Riverside 56 David Miller, Staff Scientist, Genetics Institute, Tnc., Cambridge, Mass. Clarence A. Ryan, Jr., Professor of Biochemistry, Institute of Biological Chemistry, Washington State University, Pullman M. Scott Smith, Associate Professor of Cell Microbiology, University of Kentucky, Lexington Staff Clifford l. Gabriel, StaffOff~cer, Board on Basic Biology, Commission on Life ~ . sciences AlIan R. Hoffman, Executive Director, Committee on Science, Engineering, and Public Policy Sandra Anagnostakis, Consultant, Connecticut Agricultural Experiment Station, New Haven Edward Michelson, Consultant, Uniformed Services University of the Health Sciences, Bethesda, McI. George Templeton, Consultant, University of Arkansas, Fayetteville

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Report of the Research Bnefing Panel on Biological Control in Managed Ecosystems Biological control is the use of natural or modified organisms, genes, or gene prod- ucts to reduce the effects of undesirable or- ganisms (pests), and to favor desirable or- ganisms such as crops, trees, animals, and beneficial insects and microorganisms. Man- aged ecosystems are environments managed for human benefit. They include farmland, rangeland, forests, lakes, and urban and res- idential areas. Biological control in managed ecosystems includes the manipulation and strategic introduction of organisms, genes, or gene products to influence the outcome of otherwise natural biological interactions in a manner favorable to humans. Major target pests of biological control are insects, mites, weeds, parasitic nematodes, rodents, and pathogens and their vectors. Achieving suc- cessful levels of biological control is depen- dent on fundamental knowledge of biologi- cal interactions at the molecular, cellular, or- ganismal, and ecosystem levels. Biological control has provided the under- pinning of agriculture since ancient times through practices such as crop rotation, in- tercropping, soil flooding, and tillage. Fortu- nately, most pests are still suppressed by natural biological controls such as that pro- vided by antagonists (natural enemies) and 57 self-defense mechanisms (e.g., resistance to pests) that have evolved through long asso- ciations between the host plant or animal and its pests. The era of modern biological control began about 100 years ago with the highly successful introduction of the vedalia beetle from Australia into California to con- trol the cottony-cushion scale insect pest of citrus. Nearly 90 years ago, shortly after the rediscovery of Mendel's laws of genetic in- heritance, studies of resistance to wheat stem rust provided the first indication that genes for disease resistance in plants could be transferred by conventional breeding. Because of economic forces and the lack of adequate knowledge about biological con- trols, many managed ecosystems have be- come heavily dependent on chemical pesti- cides. A "spray it" attitude developed, and even today some scientists responsible for research and extension programs tend to think of chemical controls first and of alter- native biological controls second. Thus, bio- logical control remains relatively unexplored as an active area of research. in the United States, public and private support for re- search and development applied to biologi- cal control is less than 20 percent of that for chemical control. On a global basis, of the es

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timated $16 billion spent annually on pest control, less than ~ percent is spent for bio- logical control agents. WHY BIOLOGICAL CONTROL? The use of chemical pesticides has pro- duced an increasing number of negative and nontarget effects, and pesticide residues are being found in groundwater and food. Bio- logical controls, however, have resulted in no known or only limited negative effects on the environment. Also, many pests are cle- veloping resistance to once-effective pesti- cides, making it necessary to develop new chemicals or to find effective combinations of chemicals. It is becoming increasingly more difficult and expensive to discover effective chemical pesticides. Although some pests have genetically overcome certain genes for resistance introduced in crop plants, thus far there are no examples of pests becoming re- sistant to natural enemies, pheromones, or microbial pesticides. Furthermore, many chemicals applied to control pests also de- stroy beneficial organisms and some create temporary, vacant biological niches that may then provide an opportunity for a new pest or a resurgence of the original uneasy. in con- trast, biological controls are nearly always targeted for specific pests and are therefore less likely to upset the balance among inter- acting populations. Biological control can be achieved by regu- lar or repeated applications of a control agent (e.g., a microbial pesticide) that is specific for a target pest, by a one-time or occasional in- troduction of a control agent (or genetically resistant crop cultivar) with the ability to es- tablish and keep the target pest in a state of suppression, and by enhancing the effects of indigenous natural enemies (antagonists) of the target pest or maximizing host-plant re- sistance to the pest through the use of cul- tural practices (e.g., crop rotation). Some of these biological controls may be initially less effective than many chemical controls, but 58 they are generally more stable and longer lasting. By their nature, biological controls tend to be less dependent than chemical pes- ticides on fossil energy, and many (e.g., those that achieve control in a single or only occasional application) are self-sustaining. There are many economically important pests, notably the soilborne pests and insect- vectored pathogens, for which chemical con- trols are either nonexistent or impractical. Moreover, the modern trend in agriculture toward less or no tilIage (for soil conserva- tion) and shorter or no crop rotation has fa- vored increased damage from soilborne pests. Unfortunately, the use of high-energy production inputs such as fertilizer and irri- gation are commonly increased to compen- sate for inadequate pest control or to attain greater crop yields despite the pest damage. Biological control achieved through greater knowledge of ecology and strategic intro- ductions of beneficial organisms or genetic resistance in the crop may offer the only means of stably and effectively controlling these intractable pest problems. Any gain in control over these pests is a gain for produc- tion efficiency, since yields are increased without requiring more fertilizer or water. Thus, biological control is not only an alter- native to chemical control, it also greatly helps industries such as agriculture conserve resources and become more sustainable and efficient with fewer negative effects on the environment (Table I). The development of recombinant DNA technology is unquestionably the most sig- nificant advance thus far for biological con- trol research. Recombinant DNA techniques enable scientists to understand the mecha- nisms of biological control at the molecular level in ways previously not possible. Un- derstanding the genes and gene products important to biological control opens the way for the genetic alteration of the agents carrying these genes, for the production of more useful transgenic biological control agents, and for deriving improved practices to enhance biological control.

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BIOLOGICAL CONTROL IN MANAGED ECOSYSTEMS TABLE 1 Potential Benefits from Biological Control Research F. armmg Improved pro- duction effi Agribusiness Input New high-value products for ciency leading national and to a more fa- international vorable com- markets Food Processing Decreased levels of agrichemi- cal residues in commodities for food Consumer Society International petitive stand . . . 1ng In aomes- tic and export markets Reduced health risk from agri- chemicals Plant protection for new or modified crops Low-cost food Increased qual- ity (healthful- ness) of food Cleaner, safer Improved com environment petitiveness COMPONENTS OF BIOLOGICAL CONTROL The components of biological control (Ta- ble 2) can include a pest agent used against itself (e.g., pheromones and sterile mates of insect pests), a host plant or animal we seek to protect whose defense mechanisms have been enhanced through management or ge- netic manipulation, and the pest's natural enemies and antagonists (the classic biologi- cal control agents). These components and the approaches to their management cro- vide the basis for three major biological con- tro} strategies: 1. Regulation of the pest population: biologi- cal control agents are used to regulate the pest population at or below an acceptable threshold. 2. Exclusionary systems of protection: benefi- cial microorganisms are used as a living bar- rier that excludes infection or cleters pest attack. 3. Self-defense: resistance mechanisms in the plant or animal host itself prevent or sup- press disease or pest damage. 59 All of these strategies can be demonstrated by the multiple uses of the Bacillus thuringien- sis (Bt) toxin, a protein lethal to certain in- sects. The bacterium B. thuringiensis has long been marketed throughout the worIct as a highly effective and safe microbial pesticide for use against some insect pests. With the tools of recombinant DNA technology, the Bt toxin gene has now been transferred to, and expressed in, both the common soil bac- terium Pseudomonas fluorescent and tobacco plants. Therefore, when the toxin gene is ex- pressecl in its native B. thuringiensis, it can regulate the pest population (Strategy I). When B. thuringiensis is applied as a micro- bial pesticide on plants or when the toxin gene is expressed in P. fluorescent, which grows on corn roots, it protects against insect attack by operating as an exclusionary sys- tem on the plant host (Strategy 2~. Finally, when the gene is expressed in tobacco leaves, it limits pest damage by functioning as a self-defense system within the plant host (Strategy 3~. Undoubtedly the flexibility made possible by recombinant DNA tech

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TABLE 2 Selected Examples of Biological Controls Component Strategy Regulation of the Pest Population Pheromone gossypol to control pink bollworm in cotton in Egypt, South America, and the United States Sterile males to control Exclusionary Systems of Protection Self-Defense Pest agent used against itself Natural enemies and an- tagonists (classic biolog- ical control agents) Host plant or animal screw worm in the United States Mosquitoes genetically in- capable of vectoring the malaria agent used to displace capable typesa Wasps for control of the alfalfa weevil in the United States Predatory snail for control of snail vector of schisto- somiasis agent in Puerto Rico Puccinia rust for control of skeleton weed in Aus- tralia and the United States Bacillus thuringiensis for control of certain cater- pillars-used worldwide Crotalaria grown as a trap plant; root-knot nema- tode infects this plant but does not repro- duce-minor use in the United States Avirulent strain K-84 of Agrobacterium for control of crown gall on fruit trees and ornamental plants in several countries Ice-minus strains of Pseudomonas syringae to exclude ice-nucleation- active strains from leaves of frost-sensitive plantsa Phlebia 8igantea applied to pine stumps to exclude the pine root-rot fungus Heterobasidion annosum Nonpathogenic Lactobacil- lus strains used to ex- clude Escherichia cold from the intestinal lining and protect piglets against neonatal scoursa Toxin gene from B. thurin- giensis expressed in Pseudomonas on corn roots for protection against certain soil insectsa Dense sowings of cereal- grain crops to preempt the establishment of weeds-used world- wide Mild strains of citrus tris teza virus to protect cit- rus against virulent strains of the virus in Australia and Brazil Resistance to tobacco mo- saic virus (TMV) in to- bacco plants genetically engineered to express the coat-protein gene of TMva "Immunization" (in- duced resistance) of cu- cumbers and other plant species against Colletot- richum (anthracnose) by inoculating their leaves with tobacco necrosis virusa Toxin gene from B. thurin- giensis expressed in to- bacco leaves for control of certain leaf-feeding caterpillarsa Genetic resistance to southern corn leaf blight in corn in the United States Genetic resistance to Hes- sian fly in wheat in the United States aExperimental stage only. nology will provide other new uses for other traditional biological control agents. For managed ecosystems, integrated mul- tiple biological controls are common and tend to be more effective than single-shot tactics. This may account for the relatively stable nature of biological control. A system 60 is generally developed first by using cultural practices, such as crop rotation and tillage, that maximize the effect of the natural (indig- enous) biological controls and then by intro- ducing specific controls, such as certain genes for resistance to pests, exotic enemies of naturalized pests, or inundative applica

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BIOLOGICAL CONTROL IN MANAGED ECOSYSTEMS lions of biological control agents in cases in which the natural populations are too small to be effective. SUCCESSFUL BIOLOGICAL CONTROLS REGULATION OF THE PE ST POPULATION ~ STRATEGY 1) Many (probably most) pests do not be- come economically important until they es- cape their own natural enemies or until other constraints on the pest population are eased. This generally happens when the pest is in- advertently introduced into a new environ- ment. The great majority of economically important pests in the United States, for ex- ample, were accidently introduced as a result of commerce. It has been estimated that 11 new insect pests are inadvertently in- troducec! into the United States each year. For some of these pests, successful control has been achieved by tracking down their original source and then finding and intro- clucing one or more of their natural enemies. A classic example of this is the control for the past 50 years of the Opuntia cactus in Austra- lia, following the introduction from South America of a moth (CactobZastis cactorum) that feeds on that cactus. In the United States, more than 70 candidate plant-feeding insects and plant pathogens (all fungi) have been in- troduced to control target weed species. These organisms were first selected because they are specifically adapted to feed on or parasitize the target weeds. About 14 weed species are now partly or completely con- trolled in the United States in this way. Al- most five times this number of naturalized insect pests have been controlled in the United States through the introduction of exotic parasites, predators, or pathogens. Tracking down the source of the pest can be difficult, especially if its origin is not read- ily accessible, such as in the People's Repub- lic of China,* the Middle East, or the USSR, *Henceforth referred to as "China." 61 all of which are sources of major U.S. pests. Moreover, in testing biological control agents to be used against weeds, the number of plant species that must be examined is in- creasing because of growing concern that the agent may also attack nontarget plant spe- cies. Once released, the biological control agent must be monitored for several years within the ecosystems in which the releases were made as well as within adjacent ecosys- tems. Thus far, no insect or microorganism introduced for pest control in the United States has itself become a pest. EXCLUSIONARY SYSTEMS OF PROTECTION (STRATEGY 2) A method discovered in Australia for bio- logical control of crown gall on ornamental shrubs and orchard trees is based on an ex- clusionary system that prevents the crown- gall pathogen from infecting the plant. The pathogen population may then decline through attrition, but this is secondary to keeping the plant healthy. Crown gall is caused by Agrobacterium tumefaciens, a soil bacterium that infects roots and stems through wounds such as those that occur during transplanting. In the biological con- tro} system, an avirulent Agrobacterium is used to protect wounds against the virulent Agrobacterium. This biological control agent (known as strain K-84) lacks the genetic means to incite gall formation and produces a substance that inhibits the pathogen. Bare- root transplants dipped in a cell suspension of K-84 are protected for most or all of their life. In another exclusionary type of biological control, which was developed in England, a nonpathogenic fungus is used to protect pines against root rot. This biological control agent and K-84 were the first two agents reg- istered by the Environmental Protection Agency (EPA) for use in the United States against plant cliseases. It took 10-15 years to develop each system, both of which are now used in many countries.

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Another control aimed at exclusion has the potential for protecting livestock against cer- tain pathogens. A U.S. company has devel- oped a product consisting of live cells of a nonpathogenic 7actobaciZIus fermentum, which occupies attachment sites on the in- testinal lining when introduced into new- born piglets. This preempts the attachment to the lining of the strain of Escherichia cold re- sponsible for neonatal scours. SYSTEMS OF SEEF-DEFENsE (STRATEGY 3) Plants and animals have evolved many ef- fective defense mechanisms that are subject to improvement by conventional breeding and by genetic engineering. For example, the last major epidemic of wheat stem rust in the Great Plains of the United States oc- curred over 30 years ago; this success is due to the introduction of genes for resistance as necessary according to results of annual sur- veys for virulence genes in the pathogen population. Although they are not within the scope of this report, vaccines have been the most successful biological control of dis- eases of humans and livestock. Plants have no immune system comparable to that of ani- mals, but they can be effectively protected against disease agents by inoculation with avirulent strains related to the pathogen or with a microorganism that is pathogenic to another plant. For example, the citrus tris- teza virus from Africa was introduced into South America in the 1920s anc! nearly deci- mated the citrus industries of Argentina, Brazil, and Uruguay until biological control was developed. In 1951, mild strains of the tristeza virus complex in Brazil were found to protect trees against severe strains. Com- mercial testing of these strains was begun in 196S, and by 1980, ~ million trees were pro- tected in Brazil by deliberate inoculation of seedlings with a mild strain. The same method is also used in Australia. Thus far, there is no evidence that the control is likely to break down or cause any detrimental non- target effects. RECENT ADVANCES IN RESEARCH ON BIOLOGICAL CONTROL NEW APPROACHES TO THE REGULATION OF PEST POPULATIONS Scientists are continuing to discover natu- ral enemies of pests and to find better ways to track and favor these beneficial organ- isms. Microbial pesticides are a particularly promising aspect of this classic approach and are becoming recognized by both estab- lished and start-up industries as opportuni- ties for commercial development. At least four baculoviruses are now regis- tered by the EPA for use as microbial insecti- cides, but none are commercially available in the United States. Baculoviruses are expen- sive to mass produce for large-scale distribu- tion and are slow to kill target insects. Spe- cial processes are being clesigned to decrease the cost of production, and attempts to accel- erate the kill speect are being made by genetic manipulation of the bacuTovirus genome (chromosome). For example, a toxin gene can be substituted for or inserted into a non- essential virus gene, so that the toxin is pro- duced on ingestion by the insect and kills it more quickly than the viral infection would. Microbial herbicides can rapidly and selec- tively eliminate weeds from managed eco- systems with an effectiveness similar to that of chemical herbicides. Two microbial herbi- cides are now commercially available in the United States for control of relatively minor weeds. These microbial herbicides are for- mulations of living, host-specific fungal pathogens, and were discovered around 1970. Their commerical development re- sulted from the effective collaboration of the public and the private sectors. No hazards to human health or other nontarget effects have been observed for either of these micro- bial herbicides. Several genetic traits are known to render 62

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BIOLOGICAL CONTROL IN MANAGED ECOSYSTEMS mosquitoes refractory to the transmission of the malaria parasite Plasmodium falciparum. In a novel approach to malaria control, it has been proposed that genetic manipulation could be used to transfer genes to mos- quitoes rendering them incapable of trans- mitting the parasite. These mosquitoes would be expected to compete with and re- place indigenous vector types. This ap- proach might be extended to vectors of plant viruses, but we must first amass a great deal more fundamental information, including information on vector specificity for patho- gen strains, pathogen reservoirs, and the ge- netics of virulence and transmission. MANAGEMENT OF BENEFICIAL PEANT-MICROBE ASSOCIATIONS Plants support large populations of mi- crobes (bacteria and fungi) as indigenous cosmopolitan inhabitants of their leaves, stems, and roots. These microbes may well provide the first level of defense of plants against pests. Some of the more beneficial plant-microbe associations include mycor- rhizal fungi that help the plant take in nutri- ents and water while providing some protec- tion against root disease, fungi within plant tissues (endophytes) that produce sub- stances that inhibit or are obnoxious to insect pests, and microorganisms on the leaves and roots (epiphytes) that compete with and in- hibit pathogens even before they enter the plant. These types of potential biological control agents can be applied to seeds or other planting material and therefore repre- sent significant opportunities for commer- cial development. Recent studies conducted in Australia, Canada, China, the Netherlands, and the United States reveal the potential of root-col- onizing microorganisms to inhibit or dis- place pathogens at the root-soil interface and thereby protect the root health of peren- nial and annual plants. These microorgan- isms inhibit root pathogens by producing antibiotics siderophores (compounds that 63 chelate biologically available iron), and pos- sibly substances that stimulate plant growth. One such biological control is the use of bac- terial strains of Pseudomonas fluorescens and P. putida (root-colonizing bacteria) to protect wheat roots against the soilborne fungus Gaeumannomyces graminis var. tritici. This fungus incites an important disease of wheat called "take-all. " Take-all is enhanced by the current trend toward less crop rotation and less tillage and has become the most eco- nomically important root disease of wheat worldwide. The benefical bacteria were dis- covered during basic research on the natural history of a spontaneous decrease in severity of take-all a natural biological control that sometimes follows two or three outbreaks of the disease and the continued monoculture of wheat. The bacteria thrive on wheat roots infected with G. graminis and are believed to provide this natural biological control. The most effective strains produce phenazine- type antibiotics that are strong inhibitors of G. graminis. The effective strains tested on crop plants so far occur naturally, but the genes for phenazine production are being isolated and will be available in the future to improve strains by genetic engineering. ADVANCES THROUGH UNDERSTANDING THE MOLECULAR BIOLOGY OF SEEF-DEFENsE Rapid advances are being macle in re- search on the use of natural defense systems of plants in biological control. Most if not all plants are thought to have the genetic poten- tial to protect themselves from infectious agents and from most insect and nematode pests. Damage results when the pest agent somehow circumvents or suppresses this defense mechanism by its own genetically controlled mechanisms. In addition to ge- netic improvement of resistance in plants, these defense mechanisms can be induced by inoculating the host plant with avirulent pathogens. Induced resistance in plants occurs in re- sponse to all categories of plant pathogens

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and to certain insect pests. For example, beans, cucumbers, watermelons, and musk- melons can be systemically protected against diseases caused by fungi, bacteria, or viruses by prior inoculation with agents that are ca- pable of causing only restricted infections. This protection persists for essentially the entire crop season. When certain chewing insects begin to feed on the leaves of pota- toes or tomatoes, a systemic signal triggered by small fragments of plant cell-wall material activates genes in distant leaves for synthe- sis of protease inhibitors. Insects acquire the protease inhibitors while feeding on these leaves. The insects' own digestion, physiol- ogy, and growth are then inhibited, and they cease feeding on that plant. This provides an advantage to the plant and the predators that feed on the insect pest. Investigators are now trying to transfer these genes for insect-in- duced synthesis of protease inhibitors to those plants without them. Studies of plant virus infection indicate that virus coat protein protects the plant cells against subsequent infection by a closely related strain of the virus a type of cross- protection. On the basis of these studies, to- bacco plants resistant to tobacco mosaic vi- rus (TMV) were produced by recombinant DNA technology. The TMV gene for coat protein was transferred to and expressed in tobacco and tomato plants, resulting in cross-protection without inoculating plants with the protecting virus strain. This method has also been extendecT to alfalfa mosaic vi- rus control. This approach to virus control is a major advance ant! avoids any potential risks associated with the use of mild virus strains in the field. RESEARCH OPPORTUNITIES The diversity of natural systems provides a wealth of potential biological control agents, including viruses, bacteria, and fungi. Al- though many collections of these organisms exist, adclitional research is needed to col- lect, characterize, and select the most prom . . Sing agents. In many cases, such as the ba- cuToviruses for insect control, more efficient and less costly production processes need to be cleveloped. Stabilization of biological ac- tivity during formulation and delivery is an- other need for many biological control agents. This complex field will require the in- tegration of biological and engineering skills. Biotechnology is expected to provide a means for cleveloping a more complete un- derstancling of biological interactions and for expanding genetic manipulations of organ- isms to make biological control practical on a broader scale. Opportunities for research to develop new or improved methods of biological control are virtually unTimitect. For example, my- coviruses (viruses of fungi) are associated with Toss of fungal virulence (hypoviruTence) in the fungi responsible for chestnut blight and Dutch elm disease. In France, chestnut trees are recovering where virus-infectecl (less virulent) strains of the chestnut blight fungus were introduced. The introduction of virus-infected strains has not worked in the United States, because "mating" of fungus strains must occur for the virus to be trans- mitted and there are many incompatible mating groups among the chestnut blight fungi within the country. Nevertheless, re- search on these viruses and other similar fungal pathogens deserve increased atten- tion. Opportunities for the biological control of viral diseases will be gained mainly through molecular approaches, such as genetic engi- neering to introduce resistance genes into plants, inhibiting virus multiplication with antisense viral RNA (viral RNA that is com- plementary to the messenger-sense RNA), and building on the molecular basis for cross-protection. As knowledge of how vi- ruses infect, multiply, and affect their hosts increases, so does our ability to control viral diseases. For root diseases, greater study is needecl of the pathogen-suppressive soils those sods with unique microbiological properties 64

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BIOLOGICAL CONTROL IN MANAGED ECOSYSTEMS that prevent pathogens from becoming es- tablished or from causing disease. Such soils have also been reported for certain soil-in- habiting insect pests. Knowledge of the mechanisms of suppression is providing useful new information on the ecology of such pests and is leading to the discovery of new biological control agents. There are almost unlimited opportunities to be explored in the biological control of nematodes. The pathogenic bacterium Pas- teuria penetrans is one possible biological con- tro! agent for several economically important nematodes, but as for so many other poten- tial biological control agents, there is no eco- nomic means to produce it on a large scale. Another, but less efficient biological control of nematodes is the use of plants, such as Crotalaria spectabilis, that prevent the nema- tode from reproducing. These plants might be macle to provide more efficient nematode control or could perhaps be used in insect control if they could be genetically engi- neerect to produce attractants or phero- mones. Funclamental to all areas of biological con- tro! is basic research on interspecific and in- traspecific communications, such as, how insect pests find their host plants, how plants repel insects, how natural enemies find their prey, or how individuals within the mating population of a species find or avoid one another so that the population be- comes inbred or genetically more diverse. information on local and systemic signals transmitted within plants when they are wounded or challenged by a pest will help us understand the mechanisms of recognition and defense that are important to biological control applications. Basic research in popu- l a t i o n b i o l o g y , o r g a n i s m - e n v i r o n m e n t i n t e r - actions, physiological ecology, and other areas is essential to the discovery, conserva- tion, and enhancement of future biological controls. Solving these problems in basic and ap- plied research in biological control will re- quire the continuation of traditional single 65 investigator projects; however, problems involving such complex matters as under- standing and improving mechanisms of biological control, testing and integrating systems in the field, and tracking specific or- ganisms in the ecosystem can be efficiently solved only by multidisciplinary teams of well-trainecT scientists. Such teams should include geneticists, biochemists, molecular biologists, microbiologists, physiologists, plant pathologists, entomologists, and ecol- ogists. Mathematicians should work with ecologists in modeling the complex interac- tions that occur in biological control to help provide a basis for prediction. Economists and sociologists must become involved to help guide projects from the standpoint of feasibility, acceptability, and integration with established practices. The commerciali- zation of biological control products will also require extensive research in mass produc- tion, formulation, and clelivery of these agents. WORLD STATUS OF U.S. BIOLOGICAL CONTROL RESEARCH, DEVELOPMENT, AND APPLICATION CURRENT U.S. POSITION The United States leacls the world in the discovery and reporting of biological phe- nomena related to biological control. It also ranks first in the development of recombi- nant DNA and computer technology, both of which are needed to understand and im- prove systems of biological control. How- ever, except for the conventional breeding of plants with improved resistance and the re- lease of exotic enemies of naturalized pests (classic biological control), the United States in general is not the leader in the use of bio- logical control. Many nations have indicated or demon- strated a greater commitment to under- standing biological control and to making it work. For example, research on biological

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control of plant viruses is not as extensive in the United States as it is in the Netherlands. The United States is a leader in the biological control of weeds, but Australia, a nation with only a fraction of the U.S. resources, has an effort that is almost as great. The first (and so far only) two biological agents for controlling plant pathogens registered by the EPA for use in the United States came from England ant! Australia. The Federal Re- public of Germany has a greater total effort than the United States in the biological con- troT of plant-parasitic nematodes. The United States is the leader in research on in- sect pheromones, but large foreign compa- nies are increasing their involvement in this approach to biological control. The United States along with Western Europe and Can- ada have the strongest programs in basic re- search on insect pathogens, but Brazil, China, and the USSR have the greatest expe- rience in the use of microbial insecticides. The Unitec! States has also been less suc- cessful than many countries in its efforts to assemble interdisciplinary teams of scien- tists to focus on biological control. China identified biological control as a priority in its seventh 5-year plan and has committed ma- jor resources to this area of research since 1979 (the year biological control teams were exchanged between the United States and China). In China, important pest complexes have been targeted for biological control, anc! teams of researchers are now being as- sembled to conduct the necessary research. These new Chinese research projects are based on U.S. technology. Belgium has one of the largest interclisciplinary teams for con- ducting mainly basic but also applied re- search on plant-microbe associations; few if any existing U.S. groups can compete with teams such as these. Several countries, in- cluding Canada and Great Britain, have for- malized links between public agencies and private companies as a way to assemble large enough groups to conduct research on the application of biotechnology, including bio- logical control technology. 66 U.S. PROSPECTS The United States has many advantages that could make it a world leader in the appli- cation and marketing of biological controls while also increasing its contribution of new scientific information basic to the field. it has many repositories of biological material with the raw germplasm to develop superior bio- logical controls, including those with mar- ketable components. The way is now clear in the United States for exclusive licensing of biological control agents by commercial firms, including agents developed in and patented by state or federal laboratories. The United States has an advantage in the com- position of its industrial infrastructure, which ranges from cottage industries and start-up companies to leading multinational corporations. Perhaps the single greatest advantage of the United States relative to other countries is the human resource within its network of academic institutions. No other country can match the U.S. supply of young people highly trained in molecular biology, com- puter technology, ecology, and other sci- ences fundamental to future research and development in biological control. However, competition for limited funding is so intense that agencies such as the National Science Foundation, the National Institutes of Health (NTH), and the U.S. Department of Agriculture (USDA) with interests in this area are funding only a small fraction of all proposals. Funding agencies need to direct or encourage a portion of these resources to- ward fundamental and applied studies in bi- ological control. Another major U.S. advantage is its Land Grant University and USDA/State Agricul- tural Experiment Station system. No other experiment station system in the world has the capability or experience in fielc! testing and in developing the management strate- gies to integrate biological control into agri- culture, forestry, and other managed ecosys- tems. This system can also provide links

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BIOLOGICAL CONTROL IN MANAGED ECOSYSTEMS with user communities through education and demonstrations, and employs econo- mists who can help determine economic fea- sibility. NEEDS AND RECOMMENDATIONS BASIC RESEARCH Two types of basic research needs can be identified. First is the obvious need for more basic research in areas such as ecology, ge- netics, physiology, cellbiology, and molecu- lar biology to provide adequate knowledge about biological interactions, especially those that can be modified for biological con- trol. The second need is more subtle. It con- cerns the perceptions among researchers that biological control is a narrow and ap- plied field of study. AS a result, many people working in areas fundamental to biological control have generally not thought of their research as potentially relevant to biological control. Practitioners must also adopt a broacler concept of biological control than they have in the past. SOEVING THE COMPLEX PROBLEMS A major limitation in the United States is the lack of the sustained, concentrated, and interdisciplinary effort needed to solve com- plex problems in both basic and anolied bic~- logical control research. individual investi- gators have tended to conduct short-term, descriptive research on an interesting bio- logical control phenomenon, publish one or a few papers, and then move on to another research topic. The U.S. scientific literature is replete with isolated reports of biological control, but few of these reports are actually followed-up. Because of the inherent diffi- culty and long-term nature of the work, in- vestigators lose interest, become discour- aged, or stop because their funding is too short term. The United States needs to sup- port multidisciplinary teams that have the potential for sustained research in solving 67 the complex problems related to biological control, while simultaneously continuing to support individual investigators. Such groups could be formed across departmental boundaries within a research or academic in- stitution, between two or more academic in- stitutions, or between public and private or- ganizations. in addition, training grants could be used to attract and support grad- uate students or postdoctoral associates in the more productive or successful laborato- ries or as members of a multidisciplinary team working on biological control. Career- development grants, possibly patterned af- ter the NTH model, could be used to help sus- tain young scientists for 5-10 years so that they coulc! continue their work on specific projects in biological control. MOVING RESEARCH OUT OF THE LAsoRAToRY Even under the most efficient circum- stances, the transfer of biological control re- search from the laboratory to the field is a slow process. Researchers in public-sup- ported institutions tend to avoid lengthy field tests that involve several geographic lo- cations because they are expensive and be- cause the chance of obtaining successful results has been low. The private sector, on the other hand, has generally been reluctant to invest in developing products for the nar- row, specialized markets typical of so many biological controls. The problems for biologi- cal control development are compounded by regulatory issues and questions concerning the guidelines and protocols that must be followed, whether conducting basic re- search or testing biological control agents in the field. Pharmaceutical products devel- oped through biotechnology are reaching the marketplace much faster than products for biological control, in part because of ac- celerated regulatory approval by the Food and Drug Administration. A special grants program available to both public and private researchers could be initi

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ated to support field research. Incentives for the private sector and more cooperative ties between the public and private sectors (e.g., joint ventures) are also needed to accelerate research on product development. Several small companies and three or four of the larger corporations have begun to invest in the development of biological control procI- ucts in the United States, which shows that interest in commercial development of bio- logical control is growing in the U. S. private sector. Existing state and fecleral programs on pi- Tot testing of biological control systems and on obtaining data for registration of minor- use biological control products are impor- tant. These programs could play a larger role in the transfer of technology from the labora- tory to commercial applications. The devel- opment of protocols for field research and testing should take into account the fact that cluring the 99 years of modern biological con- trol, there are few, if any, examples of a bio- logical control agent (i.e., an insect, phero- mone, microbe, or gene) having a known or significant negative effect on the environ- ment after its deliberate introduction. Thus, the existing regulations of the USDA Animal and Plant Health Inspection Service for im- portation and release of potential pests (or organisms related to pests) seem adequate for regulation of nonengineered biological control agents. In acIdition, the guidelines developed by the NTH Recombinant DNA Advisory Committee (RAC) for laboratory research with genetically engineered organ- isms seem to be an appropriate mode! for the creation of guiclelines on the field testing of genetically engineered biological control agents. Regarding final registration, there is no evidence that biological control products developed using recombinant DNA technol- ogy will require regulation that is any differ- ent from those products developed via non- engineering processes. Regulations should be based on the product's properties and not on the process used to make it. Field research with pheromones and nonengineered, non 68 pathogenic microorganisms should require protocols no different from the traditional procedures used for fielcT research on non- engineered nitrogen-fixing bacteria or new plant cultivars. CONCLUSIONS Biological control can and should become the primary method used in the United States to ensure the health and productivity of important plant and animal species. The need for alternatives to complement or re- place chemical control dictates placing an increasing emphasis on biological control re- search and clevelopment. Chemical pesti- cides are responsible for a wide array of un- acceptable negative environmental effects. For example, they tend to create fluctuating cycles of pests because they lead to selection for resistance in the pest population, and they tend to eliminate beneficial as well as harmful organisms. in contrast, biological controls have had no known or significant negative, nontarget effects; instead, they maintain the biological balance through ad- justments in the management of ecosystems and by the strategic introduction of organ- isms or their genes to influence the outcome of natural biological interactions. Advances in biotechnology greatly facilitate the devel- opment of successful new biological controls and the more effective manipulation of natu- ral forms of biological control. Major factors preventing greater use of biological controls include a lack of basic information on ecol- ogy and biological interactions, an inade- quate interdisciplinary effort to solve com- plex problems, and constraints on moving research from the laboratory to the fielcl. The development of biological contra! as the foundation of pest control in the United States is the most important challenge we face in making safe and efficient use of our managed ecosystems.