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Introduction

Biological invasions are the uncontrolled spread and proliferation of species—including vertebrates, plants, arthropods, and plant pathogens—from their native geographic ranges to new ranges. Such invasions are recurrent worldwide phenomena, and their impact on the earth is an important component of global change (Mooney and Hobbs 2000). Federal and state agencies in the United States spend over a half-billion dollars per year to respond to the influx of nonindigenous (foreign) invasive species (GAO 2000).

Nonindigenous species that threaten plant performance, survival, and reproduction are referred to as plant pests; they include insects and other arthropods, microorganisms, and plants. Over the history of the United States, plant pests have left their mark on the national landscape, spreading into natural areas (as has the invasive tree Melaleuca quinquenervia in the Everglades), increasing the frequency and intensity of fire (as has Bromus tectorum, cheatgrass, in the Intermountain West rangelands), and even pushing native species to the brink of extinction (as has Cryphonectria parasitica, the chestnut blight fungus). Some nonindigenous insects and pathogens kill their host plants directly; others reduce plant vigor, thereby increasing vulnerability to other problems.

Few nonindigenous species that arrive become invasive. For example, most of the commercially important crop and horticultural plants used in North America are nonindigenous, and most of them require cultivation for their continued survival. The most economical and productive sites for many crops are often in locales far from the native ranges of their progenitors and from the pests that attack them in their native ranges (Freeman 1991). Even under the most favorable



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Predicting Invasions of Nonindigenous Plants and Plant Pests 1 Introduction Biological invasions are the uncontrolled spread and proliferation of species—including vertebrates, plants, arthropods, and plant pathogens—from their native geographic ranges to new ranges. Such invasions are recurrent worldwide phenomena, and their impact on the earth is an important component of global change (Mooney and Hobbs 2000). Federal and state agencies in the United States spend over a half-billion dollars per year to respond to the influx of nonindigenous (foreign) invasive species (GAO 2000). Nonindigenous species that threaten plant performance, survival, and reproduction are referred to as plant pests; they include insects and other arthropods, microorganisms, and plants. Over the history of the United States, plant pests have left their mark on the national landscape, spreading into natural areas (as has the invasive tree Melaleuca quinquenervia in the Everglades), increasing the frequency and intensity of fire (as has Bromus tectorum, cheatgrass, in the Intermountain West rangelands), and even pushing native species to the brink of extinction (as has Cryphonectria parasitica, the chestnut blight fungus). Some nonindigenous insects and pathogens kill their host plants directly; others reduce plant vigor, thereby increasing vulnerability to other problems. Few nonindigenous species that arrive become invasive. For example, most of the commercially important crop and horticultural plants used in North America are nonindigenous, and most of them require cultivation for their continued survival. The most economical and productive sites for many crops are often in locales far from the native ranges of their progenitors and from the pests that attack them in their native ranges (Freeman 1991). Even under the most favorable

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Predicting Invasions of Nonindigenous Plants and Plant Pests growing conditions, most crops fail to become invasive or even naturalized (that is, persistent but in low numbers) in new ranges. The species that do arrive in the United States and become invasive, including the pests of nonindigenous crops, collectively affect the safety of our supply of food, fiber, timber, and water and the health of our domesticated animals and even humans. The cost of such invasions is probably incalculable. The aggregate figure for crop and timber losses and for the use of herbicides and pesticides to fight invasive species exceeds $100 billion per year, but this figure does not include the direct and indirect economic and ecological costs of invasions in ecosystems that are less intensively managed, such as forests, pastures, wetlands, and other wilderness areas (Pimentel et al. 2000). As a result of the magnitude of the problem, scientists, crop producers, environmentalists, and public agencies are exploring ways to combat plant pests, beginning with preventing their entry into the United States. What might seem to be a straightforward endeavor is actually difficult. Regulating the arrival of nonindigenous species remains one of the most challenging tasks facing plant regulatory agencies today, because a major component of the global economy involves the transport of agricultural products, including the transfer of living organisms. Not only are agricultural products (such as grain, animal products, lumber, plant fibers, and cut flowers) being moved worldwide in unprecedented volume, but the use of imported germplasm that would give rise to these products in vast new markets is also increasingly widespread. TROUBLE ON THE BORDER The Animal and Plant Health Inspection Service (APHIS) of the United States Department of Agriculture (USDA) is responsible for preventing the introduction of plant and animal pests along human-mediated pathways. It carries out this mandate by prohibiting importation of known pests and by regulating the importation of commodities (such as fruits and vegetables), plants, and plant propagation materials that might harbor pests. APHIS agents at seaports, borders, and airports intercept restricted items such as food carried by tourists, and detect known pests that contaminate commodities, packing materials, and shipping containers. Although its monitoring activities in 1999 resulted in two million interceptions, which prevented the introduction of an estimated 53,000 plant pests (USDA 2000), the agency has the capacity to examine less than 2% of the cars, trucks, ships, and airplanes that bring products and people into the United States. APHIS devotes much effort to evaluating the possibility that harmful pests will be contaminants in imported commodities and the significance of the economic or environmental damage that could result if these pests were introduced. Such evaluations are conducted on the basis of the probabilities of transportation and establishment and constitute the agency’s assessment of the risk of introductions. Risk assessment is the basis of APHIS decisions to permit or restrict the

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Predicting Invasions of Nonindigenous Plants and Plant Pests importation of a commodity or to impose phytosanitary requirements, such as fumigation, that could exterminate hitchhiking pests. Risk assessments are most reliable when the identity and biological characteristics of a pest likely to be associated with a commodity are well documented and when the availability and vulnerability of potentially affected plants and their communities in the United States are known. Risk assessments are less reliable when it is not known which species might accompany a commodity or when known organisms are likely to be present but have an unknown capability to invade ecosystems and to harm plants in the United States. Even when much is known about the biological characteristics of a species in its native range, it can be difficult to predict the results of its entry into a new range. Intentional introductions of nonindigenous species for biological control of some specific pest, for example, have on occasion resulted in the introduced species’ unexpectedly attacking species in addition to the targeted ones. Biological control species sometimes compete with and displace native species and have other unexpected effects (Louda et al. 1997, Lockwood et al. 2001). Consequently, release of these organisms requires careful prerelease screening and postrelease evaluation. A parallel problem is posed by the importation of nonindigenous plant cuttings and seeds for horticulture and other uses. Some plants known to be invasive are on the federal noxious weed list, and these species are consequently prohibited from importation. If no information on their invasive potential is available, propagative materials are allowed to enter virtually without restriction. The importation of propagative materials and commodities in the absence of definitive knowledge of their invasiveness weakens or even undermines the national system of plant protection. Even at the outset of any examination of these issues, it is clear that the predictability of invasiveness requires more scientific information and more effective use of existing information. The capability to use scientific principles and procedures to make such a prediction is urgently needed, not only to protect plant life, but also to fulfill U.S. commitments under international trade agreements. The United States helped to establish the World Trade Organization (WTO) in 1995 to liberalize world trade opportunities. With more than 142 nation members, WTO maintains a code of trade rules and is a forum for discussing and adjudicating trade disputes. Disputes between nations can involve market access, export subsidies, domestic support schemes, and the sanitary and phytosanitary measures used by nations to dictate whether foreign goods may enter their borders on the basis of concerns for the health and safety of their citizens, plants, and animals. Before the creation of WTO, no international rules distinguished legitimate importation restrictions from trade barriers erected under the guise of protecting health or safety. Under WTO, the exclusion of any trade item must have a scientific basis (USDA/FAS 1999). The requirements apply as well to controls that the United States places on the movement of materials to protect this country from invasive plants and plant pests.

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Predicting Invasions of Nonindigenous Plants and Plant Pests To clarify the basis of claims related to plant health, WTO, through the International Plant Protection Convention, sets international standards for phytosanitary measures in trade. Each country may establish its own standards, even if they are more conservative than the international ones, but they must be based on risk assessment and be justifiable scientifically. The United States, as with other WTO members, is expected to benefit substantially from increased access to new markets for exports and from lower import prices for agricultural and forestry commodities. Trade liberalization in agriculture alone is expected by 2005 to raise world income by as much as $5trillion and almost double the value of U.S. exports and imports (USDA/FAS 1999). However, trade liberalization increases correspondingly the likelihood that some of the hundreds of thousands of species of plant pests not yet found in the United States will someday arrive here. APHIS is responsible for making regulatory decisions that simultaneously facilitate trade, comply with international laws, and reduce the risk of disseminating plant pests. That responsibility is daunting; APHIS needs whatever scientific tools are available to assist regulators in meeting potentially competing objectives. SCOPE OF THIS STUDY AND STRUCTURE OF THE REPORT APHIS asked the National Research Council’s Board on Agriculture and Natural Resources (BANR) to review scientific knowledge about the characteristics of nonindigenous organisms, environments, and the process of invasion that could be used to refine inputs into its risk assessments, identify potential invaders, and guide the strategic allocation of its resources to safeguarding plant life in the United States. BANR established the Committee on the Scientific Basis for Predicting the Invasive Potential of Nonindigenous Plants and Plant Pests in the United States, which comprises experts in invasive plants, plant pathology, entomology, horticulture, risk assessment, ecology, and population biology. The committee was charged to consider the available relevant historical and scientific data on plant, pathogen, and arthropod invaders and on the characteristics of plants that facilitate or impede invasions and to prepare a report that evaluates how scientific principles and procedures could be used to predict the invasive potential of nonindigenous plant pests. The committee met four times over a 12-month period, examined the scientific literature, and spoke to numerous experts on biotic invasions of agricultural and natural ecosystems. In preparing its report, the committee undertook a four-stage analysis of the invasion process: the introduction of a nonindigenous species (immigration), its persistence at some threshold level (establishment), its proliferation and geographic spread (invasion), and finally the manifestation of its adverse effects on its new environment (impact). Chapter 2 deals with the factors that have historically influenced the accidental or intentional introduction of species into an area.

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Predicting Invasions of Nonindigenous Plants and Plant Pests Although many nonindigenous species arrive in new ranges, few persist; Chapter 3 examines this important issue. Understanding the processes that allow persistence can have important implications for restricting the establishment of nonindigenous species before they become invasive. In Chapter 4, the committee examines the forces that facilitate or impede the proliferation and geographic spread of a plant pest, a stage at which a species can be said to be invasive. For most organisms, this stage is often the first process that can be observed directly; arrival and persistence usually occur without detection. Invasion is also the stage in which organisms can exhibit adverse impacts on the surrounding plant life and the ecosystem in general. The impacts of invasions have received the most attention by researchers and are examined in Chapter 5. There is some overlap between components of this analysis, but the approach nonetheless serves as a common denominator among taxa, whether they are plants, arthropods, or plant pathogens. Even in the face of terminological, theoretical, and methodological differences among the scientific disciplines that study these organisms, the conceptual model allowed us to acknowledge the differences and facilitate their integration. In Chapter 6, the committee examines predictive methods and provides its own set of questions as a framework for using scientific information to predict the invasive potential of plants and plant pests. The chapter summarizes the ability to use scientific principles and processes to predict invasiveness and discusses implications of that capability for risk assessment. Summaries of key scientific findings are listed at the ends of Chapters 2-6. In Chapter 7, the committee presents its overall conclusions and makes recommendations regarding research that is needed to improve the ability to predict invasiveness. This report focuses on the threats of introduced plant pests to the plant resources of the United States. It does not explicitly include genetically modified organisms, although much of the same analysis would be relevant. Vertebrate pests are not included in the committee’s charge, and aquatic plant resources, such as aquatic ecosystems and submerged aquatic vegetation, have largely been excluded. Otherwise, all forms of vascular plants–whether in agriculture, in forestry, or in natural areas in the United States–are topics of concern in this report.