Pests—arthropods, weeds, and pathogens—have been, are, and will continue to be major constraints to agricultural production and forestry in the United States and throughout the world. Synthetic chemical pesticides were introduced in the 1940s and used widely on agricultural crops in the hope that they would control agricultural pests. It is now clear that their use has some unfortunate consequences. Many consumers believe that trace residues of synthetic chemicals in food are undesirable and represent a significant food safety risk. In some cases, undesirable environmental impacts of synthetic pesticides have caused consumers to oppose the use of these materials in agriculture and caused governments to regulate or outlaw their use.
Pests develop resistance to synthetic chemical pesticides, just as microbial pathogens of humans develop resistance to antibiotics. In fact, pest resistance currently limits the efficacy of many insecticides, fungicides, and herbicides; and there are pests such as plant-parasitic nematodes and bacteria for which no effective pesticides are available. Many synthetic chemical pesticides are broad-spectrum, killing not only arthropod and pathogen pests but also beneficial organisms that serve as natural pest-control systems. Without benefit of the natural controls that keep pest populations in check, growers become increasingly dependent on chemical pesticides to which pests may eventually develop resistance. Thus there is an urgent need for an alternative approach to pest management that can complement and partially replace current chemically based pest-management practices.
Pest-management strategies can be viewed in context of whole-farming systems. In whole-farming systems, pest-management methods are integrated into
other management components of agronomic systems such as crop fertilization, cultivation, cropping patterns, and farm economics. Such alternative farm-management strategies that promote soil and plant health, and water quality were recommended by the National Research Council in their report Alternative Agriculture (National Research Council, 1989b).
CULTURAL AND BIOLOGICAL APPROACHES TO PEST MANAGEMENT
Ecologically based pest management (EBPM) is recommended as a profitable, safe, and durable approach to controlling pests in managed ecosystems.
Early agriculturalists faced serious pests that decimated crops. Through trial and error, they implemented practices that challenged such pests. Successful strategies predominantly were those that served to maintain the ecological balance of the region and the natural balance of agricultural pests and their enemies. This committee believes that such practices, combined with the advanced biological technologies now available, are the most logical approach to developing a profitable, safe, and durable (long-lasting and self-maintaining) approach to pest management. The systems, hereafter identified as ecologically based pest management (EBPM), as outlined by this committee, rely primarily on inputs of pest biological knowledge and secondarily on physical, chemical, and biological supplements for pest management. The EBPM systems will be built on an underlying knowledge of the managed ecosystem, including the natural processes that suppress pest populations. It is based on the recognition that many standard agricultural practices disrupt natural processes that suppress pests. In contrast to standard practices that disrupt and destabilize the agroecosystem, agricultural practices recommended by EBPM will augment natural processes. These practices will be supplemented by biological-control organisms and products, resistant plants, and narrow-spectrum pesticides.
The concept of EBPM builds on the cultural and biological approaches to pest management that were in use prior to the widespread application of synthetic chemical pesticides. Many practices, such as crop rotation, fallowing, intercropping, and incorporation of organic matter into soils, served to conserve and foster populations and activities of biological control agents that were indigenous components of traditional agricultural ecosystems; nevertheless, pest outbreaks and crop and animal disease epidemics did occur. Through trial and error, early agriculturalists discovered and used natural substances, beneficial organisms, and selected resistant plants to their benefit. These early agriculturalists laid the foundation for pest management based on the biology of the ecosystem. The EBPM system builds on these earlier approaches but uses advanced technological tools and methodologies to improve the knowledge base and, where necessary,
includes inputs—chemical, biological, or physical—that meet the objectives of safety, durability, and profitability.
The objectives of EBPM are the safe, profitable, and durable management of pests that plague agricultural production and forestry. Examples of EBPM systems currently in use are included in this report to demonstrate the potential of EBPM to meet the goals of safety, profitability, and durability, but it is now necessary to move EBPM beyond isolated instances and into the mainstream of pest management. Wide-scale implementation of EBPM will require generating a substantial ecological knowledge base of agricultural and forest ecosystems and development of regulations and oversight consistent with the risks of the inputs. The process of creating the necessary knowledge base must begin now because the information needed to form the foundation of EBPM is lacking. Knowledge must then be transferred effectively to growers and producers to enable the implementation of EBPM. The need to generate the necessary knowledge and to develop ways to facilitate its transfer, in addition to the need to develop appropriate regulations, are emphasized in this report because these are viewed as major factors that currently limit implementation of EBPM.
Early integrated pest management (IPM) innovators should be recognized for conceiving a framework for an integrated approach to arthropod, weed, and pathogen pest management. IPM strives to manage pests using ecological principles of natural pest mortality factors; pest-predator relationships; genetic resistance; and cultural practices (National Research Council, 1989b). This theoretical basis of IPM is similar to EBPM.
The practice of IPM, unfortunately, is not always consistent with the theory of IPM. The focus of early IPM programs was devoted to control of insects, setting a precedent for the focus of IPM on arthropod pest management. In many cases, this management was limited to pest scouting and precise applications of insecticides. Consequently, this focus has been at the expense of IPM of weed and pathogen pests.
The ecological concepts of the IPM framework are the departure point for this new information-rich management strategy. EBPM will rely on an improved knowledge base of the complex ecological processes that occur in plant production.
Safety, Profitability, and Durability
The three fundamental goals of EBPM are (1) safety, (2) profitability, and (3) durability. The committee considers all three of these goals essential to developing and implementing EBPM strategies.
EBPM is a total systems approach designed to have minimal adverse effects on nontarget species and the environment because biological controls are limited by their specificity with respect to the target pest organism or by their distribution or persistence in the environment. In addition, the acute and chronic toxicities associated with conventional chemical pesticides generally have not been found
with biological-control organisms and products, although there can be risks such as allergenic reactions with multiple exposure. However, unlike new synthetic chemicals, whose effects on living organisms and the environment may be difficult to predict, with biological organisms and molecules, there is in most cases an experience base on which environmental risks can be assessed.
For EBPM to be successful, it must also be profitable for the grower. Growers demand safe, economical, and effective tools that provide long-term management of pests; and these needs must be met before growers will implement EBPM's new tools. Because producers will implement only those pest control methods that lower economic risks and enhance profits, they will insist on assurances that biologically based tools are cost-effective and provide consistent responses. Alternative management strategies may indeed be less expensive than chemically based methods, but information to determine relative costs is not available and needs to be researched.
EBPM strategies also must be long-lasting to have a positive impact on crop protection. Work by crop breeders to increase cultivar resistance to arthropods and pathogens is constantly being undone by pests that overcome the plant's resistance. As new pest-resistant cultivars are introduced into a cropping system, biotypes of organisms that overcome this host resistance can predominate. Similarly, pesticide resistance limits the durable use of chemical pesticides; and resistance of pests to biological-control products and organisms can also occur. Decreasing the pest's rate of development of resistance to new inputs is essential for the durability of EBPM.
Given the funding to build the necessary knowledge base, scientists can further develop ways to modify the deployment of biological-control organisms, products, and resistant cultivars to delay the onset of resistance. A large annual research and development investment of more than $500 million continues to support the production of organic pesticides; an increased investment in research of biological processes will be needed to support the development of EBPM.
DEVELOPING A KNOWLEDGE BASE
A national research agenda, both general and cross-cutting, should be developed to identify broad areas of ecological research that promise to yield the critical information needed to accelerate progress in EBPM.
Implementation of EBPM will require more ecological and economic information than do current pest-management systems. With conventional pest-management systems, growers rely primarily on synthetic chemical inputs to control a broad spectrum of pests. With EBPM, growers and pest managers depend on knowledge of pest biology and economic feasibility of pest control options. Because numerous organisms can cause crop damage and reduce yields, growers need information about many pest-management alternatives to make an informed decision.
Understanding the Interactive Processes of Ecosystems
Because pest management should be based on knowledge of agricultural and forest ecosystems, researchers should focus on developing a better knowledge base of the interacting components and processes that characterize agricultural and forest ecosystems.
An agricultural or forest ecosystem consists of a dynamic web of relationships among crop plants or trees, herbivores, predators, disease organisms, weeds, etc. These organisms constantly evolve and respond to each other, creating a diverse, complex, and ever-changing environment. The occurrence of a pest in a particular agricultural field is not an isolated event and, as such, must be studied in relation to the larger geographic region.
EBPM uses knowledge of interactions among pests and naturally occurring beneficial organisms to modify cropping and forestry systems in ways that reduce rather than eliminate damage caused by pests; thus, EBPM is designed to enhance the inherent ecological strengths of the system. External inputs—a continuum of biological, physical, and chemical tools—would be added only if they promote the long-term environmental health of soil biota, crops, and other organisms of agricultural and forestry production systems. In contrast to the current approach, which often relies predominantly on broad-spectrum chemical methods, with EBPM, new inputs—natural or synthetic—must target specific pests and minimize disruptions to the managed ecosystem.
Research is needed to identify organisms and their functions in the ecosystem. Little is known about the diverse competitors, predators, and parasitoids that reside in soil and plant environments; yet, beneficial organisms that control pests within their native environments have been found in these habitats. Researchers are discovering that organisms in a cropping system interact in many ways—through competition, molecular signaling, toxicity, host selection, predation, and antibiosis. Understanding the processes of these interactions can lead to science playing a decisive role in controlling pest populations and contributing to the stability of natural systems. Based on these discoveries, researchers are developing new pest-management strategies to hold pest populations in check.
EBPM requires development of biological-control organisms that can be used to mimic natural processes of pest suppression. Identification of biological-control organisms is leading to commercialized products that can effectively suppress specific pests with increased safety to human health and the environment. Biologically based supplements will include live biological-control organisms (for example, beneficial insects, nematodes, microbes, and viruses), the application of specific biological-control products (pheromone attractants and microbial toxins), and development of genetically improved plants (disease-resistant cultivars). Both traditional and molecular methods will be used for genetic improvement of crop plants and beneficial organisms.
The Need for Multidisciplinary Ecosystem Research
The complexity of managed ecosystems necessitates coordinated multidisciplinary and interdisciplinary research to develop and implement EBPM.
The knowledge needed to build the foundation of EBPM will come from nearly all disciplines of both the biological and social sciences and will require research from molecular to landscape levels. The committee has identified eight broad research areas that should receive priority:
ecological research of managed ecosystems,
research of behavioral, physiological, and molecular mechanisms affecting EBPM,
identification and conservation of resources necessary for EBPM,
development of better research and diagnostic techniques,
development of ecologically based crop protection strategies,
research on implementation of EBPM,
research on socioeconomic issues of EBPM, and
development of new institutional approaches to encourage interdisciplinary cooperation.
Although individual research will continue to be important in developing the information and conceptual framework for EBPM, interdisciplinary research and cross-disciplinary flow of information will be needed. Institutional barriers that fail to foster interactive endeavors will continue to impede research and training needed to build the fundamental knowledge necessary to develop EBPM. A professional society that unifies scientists involved in all aspects of agricultural research, development, and implementation can lead efforts to achieve EBPM.
New Research Methods
Researchers should devise new methods to study, monitor, and evaluate agricultural and forestry ecosystem processes and to develop effective pest-management tools.
New methods must be developed to study, monitor, and evaluate pests and potential biological-control organisms in order to expedite the acquisition of knowledge needed to implement EBPM. The lack of effective methodologies to characterize ecological systems hampers research aimed at generating the conceptual framework of agricultural and forestry ecosystems on which EBPM will be based. The development of molecular techniques useful in genetic manipulation of plants, insects, and microorganisms provide an unprecedented opportunity for optimization of host plant resistance or biological-control activity; but these techniques must be amended substantially to expand their usefulness from model
organisms to the diverse groups of plants and biological-control organisms that will comprise EBPM. Researchers, pest control advisors, and growers will require sophisticated methods for tracking and monitoring populations of pests and biological-control organisms to optimize timing of applications of biological or chemical supplements and to avoid unnecessary risks associated with the application of supraoptimal concentrations of these supplements. New site-specific techniques such as geographic information systems (GIS) and remote sensing already are useful in geographic applications and can potentially be useful in tracking and monitoring pest movements.
Implementation research is needed to facilitate the transfer of technology from researchers to pest managers in the field. Experience with IPM indicates that the complexity of EBPM may become a major limitation to its implementation. Laboratory discoveries must be moved into agricultural practice to increase adoption of EBPM. Pest suppression activities of biological-control organisms can be demonstrated in the field to growers and pest managers, emphasizing the site-specific nature of EBPM methods. Growers need analyses that compare benefits and costs of pest-management methods before they can make informed decisions. Scientists must devise strategies to supply growers with sufficient biological-control inputs and conserve valuable biological-control resources, thus increasing the longevity of EBPM. Implementation of EBPM will be advanced only if information is shared among scientists, suppliers of agricultural products, pest managers, and growers.
In the past, growers relied primarily on cooperative extension agents to provide pest-management education. The public sector should continue to play an important role in training pest-management personnel and consultants. With increasing knowledge and time requirements needed to implement EBPM strategies, information will need to be synthesized to increase its accessibility. Independent consultants will play a more important role in the transfer and synthesis of information, and the increase in automated information sources will facilitate information transfer at all levels.
Transfer, synthesis, and simplification of information among growers, suppliers, and public agencies will speed the successful development and implementation of EBPM; and public investment to develop and approve registration of biological-control organisms can assure availability of safe and effective pest-management tools. Extension scientists, in particular, need to become active and interested participants to make EBPM successful. Cooperative activity among growers, suppliers of agricultural supplements, and investors as well as the scien-
tific community would lead more quickly to breakthroughs such as discoveries of ways to delay development of pest resistance and, thus, reduce pest-management costs. Such cooperative efforts among all necessary communities will benefit stakeholders and society at large.
PUBLIC OVERSIGHT OF ECOLOGICALLY BASED PEST MANAGEMENT
Wide-scale implementation of EBPM could require thousands of commercialized biological-control organisms, products, and resistant cultivars, each of which could be quite specific with respect to the target pest as well as the cropping system to which each could be applied. Public oversight is required to ensure that potential risks to human health or the environment are properly assessed and managed, thereby promoting public acceptance of the use of biological-control organisms and products or resistant cultivars. In assessing risk, public agencies must use appropriate criteria and methods to avoid delays and expedite reviews. In the same way that public funds are used to obtain registration of minor use pesticides, there is a need to encourage the registration of biological-control organisms with limited market potential.
Evaluation of risks associated with deployment of biological-control organisms and products and resistant plants should be based on evidence relative to both the type of organism or product and its method of deployment.
Humans will come into contact with biological-control organisms, biological-control products, and resistant cultivars during production and application and through exposure to organisms or residues that persist on crops and in the environment. An advantage of the tools of EBPM is that many have negligible toxicity to humans; nevertheless, their potential risks to human health must be assessed. Large-scale production of biological-control organisms and products should minimize human exposure to bacteria, fungal spores, proteins, and other reactive materials. Resistant cultivars, altered by classical breeding or genetic engineering, may affect human health if greater amounts of toxic metabolites are produced in the edible portion of the plant. Similarly, biological-control products and metabolites produced by biological-control organisms should be evaluated for human toxicity.
Much has been learned from prior releases of biological-control organisms; this information can provide a basis for assessment of future risks associated with the use of biological-control organisms in agriculture and forestry. Biological control has a credible history; in the many years in which biological-control organisms and resistant plants have been used in agriculture, negative effects on
nontarget organisms or on plant health have been observed in very few cases. If a biological-control organism is unfamiliar or there is uncertainty about the environment into which it is introduced, however, careful evaluation must precede its introduction. Nontarget organisms closely related to the pest are most at risk from parasitism or predation by introduced natural enemies, although quantification of such risk requires more evaluation. There is also a small possibility of exacerbating pest problems following introduction of biological-control organisms or resistant plants. For example, progeny resulting from genetic exchange between a resistant plant and indigenous plant species could persist and could possibly become troublesome, invasive components of agricultural ecosystems. Although the long history of deployment of resistant plants indicates that such problems occur extremely rarely, the risk of environmental effects resulting from the use of resistant plants in agriculture must be assessed. Unknown consequences of genetic exchange between biological-control agents and indigenous organisms also may exist, but field evaluation can assess the likelihood and effects of these events in a natural setting.
Experience and Experimentation
All experience including that gained from the natural occurrence of the biological materials and their toxicity and field testing should be fully considered in regulatory review of new organisms or products.
Knowledge of their origin in the biosphere provides an appropriate experience base for most biological organisms and molecules. For all EBPM candidate organisms or products, this experience base should be combined with experimentally derived data as well as data about organisms that are closely related taxonomically or functionally as evidence to assess risk. The evidence should be organized so as to address the potential risk criteria specific to the organism, product, or plant and its deployment. Experience with these manifestations of risk will be useful in evaluating EBPM strategies.
The potential exists for managing pests in an agricultural or forestry ecosystem using a wide range of biological controls; this, however, creates the necessity of setting oversight requirements for each biological product or organism. The task of risk assessment can be expedited by drawing on experiences with similar biological-control organisms or products, pests, and agricultural and forest ecologies; and as this knowledge base expands, oversight requirements can be adjusted accordingly.
Experience, experimentation, and expert opinion should direct oversight attention to broad-spectrum organisms, products, or resistant plants and uses on major acreage crops where risk impact could be greatest. At the same time, effective review will exempt or remove from oversight those organisms, products, or resistant plants for which accumulated experience indicates low risk.
The Need for Guidelines
The U.S. Environmental Protection Agency and the U.S. Department of Agriculture, both currently responsible for oversight or pesticide regulations, should develop and publish a guide to risk criteria, data requirements, and oversight procedures that apply to importation, movement, introduction, testing, and release or registration of biological-control organisms or products.
Inconsistencies in the existing laws and regulations are barriers to effective, efficient oversight of biological-control organisms, products, and resistant plants. Complexities and anomalies of the current regulatory system may be attributed to the overlapping jurisdiction of several agencies, the diversity of organisms to be regulated, and the attempt to make the decision-making ''template" developed for registration of conventional chemical pesticides applicable to biological controls. It is essential that regulatory agencies assess risk using criteria and protocols that are appropriate to biological tools in contrast to broad-spectrum synthetic chemical pesticides. This will provide an appropriate level of oversight and minimize costs imposed by duplication of oversight and reporting requirements.
A NEW ERA
This committee believes that it is necessary to refocus objectives from pest control to pest management based on maintaining natural ecological balances. The problems of consumer and societal acceptance, safety, pest resistance, and economic cost dictate the need for immediate change in current pest-management practices that rely on short-term, broad spectrum solutions to solve major pest problems. There needs to be a paradigm shift in pest-management theory from managing components or individual organisms to an approach that examines processes, flows, and relationships among organisms. Major barriers must be overcome if EBPM is to be successful. It cannot be overemphasized that collaboration of scientists in a range of disciplines, suppliers of agricultural products, educators, and growers is critical to the success of EBPM. Many believe that the consultant/farmer linkage will be where knowledge, decision making, and action take place. The lack of such collaboration contributed to a retreat from the principles of IPM. This committee sees an opportunity to move beyond IPM and into an information-rich era in which collaborative efforts break down current barriers among the disciplines, institutions, and philosophies to achieve ecologically based pest-management solutions that are safe, profitable, and durable.