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Risk Analysis, Vol. 24, No.

4, 2004

Risk Assessment for Invasive Species


Mark C. Andersen,1 Heather Adams,1 Bruce Hope,2 and Mark Powell3

Although estimates vary, there is a broad agreement that invasive species impose major costs on the U.S. economy, as well as posing risks to nonmarket environmental goods and services and to public health. The domestic effort to manage risks associated with invasive species is coordinated by the National Invasive Species Council (NISC), which is charged with developing a science-based process to evaluate risks associated with the introduction and spread of invasive species. Various international agreements have also elevated invasive species issues onto the international policy agenda. The World Trade Organization (WTO) Sanitary and Phytosanitary (SPS) Agreement establishes rights and obligations to adhere to the discipline of scientic risk assessment to ensure that SPS measures are applied only to the extent required to protect human, animal, and plant health, and do not constitute arbitrary or unjustiable technical barriers to trade. Currently, however, the eld of risk assessment for invasive species is in its infancy. Therefore, there is a pressing need to formulate scientically sound methods and approaches in this emerging eld, while acknowledging that the demand for situationspecic empirical evidence is likely to persistently outstrip supply. To begin addressing this need, the Society for Risk Analysis Ecological Risk Assessment Specialty Group and the Ecological Society of America Theoretical Ecology Section convened a joint workshop to provide independent scientic input into the formulation of methods and processes for risk assessment of invasive species to ensure that the analytic processes used domestically and internationally will be rmly rooted in sound scientic principles.
KEY WORDS: Invasive species; risk assessment; theoretical ecology

1. BACKGROUND The entry, establishment, and spread of nonindigenous species in new environments can cause major economic damage, irreversible ecological changes, and signicant public health impacts. While many nonindigenous species provide benets in their new environment (e.g., the major crop plants), or are considered benign, others are regarded as detrimenDepartment of Fishery and Wildlife Sciences, New Mexico State University, Las Cruces, NM 88003-003, USA. 2 Oregon Dept of Environmental Quality, Portland, OR 972152654, USA. 3 USDA Ofce of Risk Assessment and Cost Benet Analysis, Washington, DC 20250, USA. Address correspondence to Mark C. Andersen, Department of Fishery and Wildlife Sciences, New Mexico State University, Las Cruces, NM 88003-003, USA; manderse@nmsu.edu.
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tal and therefore invasive. In many cases, the classication of nonindigenous species is complicated by offsetting benets from damages. Invasive species such as the zebra mussel (Dreissena polymorpha), which can clog water pipes for electric power plants and municipal and irrigation water supplies, cause tangible economic damages. Invasive species also may diminish the provision of nonmarket environmental goods and services (e.g., water quality). Nonindigenous invasive species can impact native ecological communities directly (through predation, grazing, parasitism, infection, competition, or hybridization). Their impacts also may be brought about indirectly through modication of ecosystem functions (e.g., by altering re regimes, hydrology, nutrient cycles, and energy ows). The introduction of nonindigenous infectious agents (e.g., West Nile virus) 787
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2004 Society for Risk Analysis

788 and/or exotic disease vectors present risks to public health and to the health of domestic and wild animal and plant populations. Taken alone, the estimated economic damages resulting from individual invasive species can be signicant. For example, since its introduction, the unpalatable weed, leafy spurge (Euphorbia esula), has spread to more than 5 million acres of rangeland in the northern Great Plains, causing estimated production losses, control expenses, and other economic damages in excess of $100 million per year. The total cost of the eradication program for citrus canker (Xanthomonas campestris pv. citri) is expected to exceed $200 million. The U.S. Department of Agriculture 2001 scal year budget for invasive species activities alone exceeded $580 million. Recent studies that have attempted to estimate the total national impact of invasive species also suggest that the overall magnitude of annual economic change exceeds the federally-dened threshold of $100 million per year for major economic impacts.(14) Invasive species may cause irreversible changes to ecological communities by altering the composition and abundance of native species, in some cases, to the point of extinction. The Ofce of Technology Assessment(2) provides a discussion of the evidence implicating invasive species in the extinction or endangerment of species native to the United States. One of the few accepted generalizations about the ecological effects of biological invasions is that the greatest impacts occur when a nonindigenous species performs an entirely novel function in the recipient community. Examples include invasions of oceanic island communities by mammalian predators and the invasion of nitrogen-xing plants in regions with nitrogen-poor soils.(5) In addition to many of the problems besetting economic impact assessments, ecological impact assessment of invasive species is further hindered by the lack of a common currency for measuring and expressing changes, by uncertainty or disagreement about what constitutes an adverse ecological impact, and by the difculties of predicting the nature and amounts of impacts. 2. INVASIVE SPECIES ON THE POLICY AGENDA The National Invasive Species Council (NISC) coordinates the U.S. domestic effort to manage risks associated with invasive species. The NISC, established in 1999 by Executive Order 13112, consists of eight federal departments with leadership roles for

Andersen, Hope, and Powell invasive species issues and is co-chaired by the Secretaries of Agriculture, Interior, and Commerce. E.O. 13112 requires a science-based process to evaluate risks associated with the introduction and spread of invasive species, and a coordinated and systematic riskbased process to identify, monitor, and interdict pathways that may be involved in the introduction of invasive species. The NISC 2001 National Management Plan calls for development of a risk analysis system for nonnative species by 2003.(1) The issue of invasive species has been elevated onto the international trade and environmental policy agendas through a variety of international agreements and by conspicuous incursions of nonindigenous pests. An obvious example of such a pest is the Asian longhorned beetle (Anoplophora glabripennis), which has infested hardwood trees in U.S. metropolitan areas. Under the World Trade Organization (WTO) Sanitary and Phytosanitary Agreement (SPS Agreement), members of the international trading community have agreed to adhere to the discipline of scientic risk assessment. This is to ensure that the SPS measures are applied only to the extent required to protect human, animal, and plant health, and do not constitute arbitrary or unjustiable technical barriers to trade (http://www.wto.org/english/ tratop e/sps e/sps e.htm). The SPS Agreement recognizes the World Organization for Animal Health (Ofce International des Epizooties, or OIE) and the international and regional organizations operating within the framework of the International Plant Protection Convention (IPPC) as the international standard-setting bodies for animal health and phytosanitary measures, respectively. The scope of OIE guidelines for terrestrial and aquatic animal health risk assessment includes the potential public health and environmental consequences of pathogenic agents (http://www.oie.int/eng/en index.htm). The IPPC Interim Commission on Phytosanitary Measures recently initiated efforts to develop standards for conducting plant pest risk analysis for environmental hazards, to explicitly address risks to nonagronomic ecosystems, where plant pests include plants, animals, or pathogenic agents directly or indirectly injurious to plants or plant products (http://www.fao. org/WAICENT/FaoInfo/Agricult/AGP/AGPP/PQ). Invasive species issues are also being elevated onto the international agenda via the Convention on Biological Diversity (CBD), which urges countries to prevent the introduction of and to control or eradicate nonnative species that threaten ecosystems, habitats, or species (http://www.biodiv.org). The CBD

Risk Assessment for Invasive Species Biosafety Protocol (known familiarly as the Cartegena Protocol) requires decisions regarding the international movement of living modied organisms to be subject to risk assessment (http://www.biodiv.org/ biosafety). Article 196 of the United Nations Convention on the Law of the Sea (UNCLOS) calls for measures to prevent, reduce, and control the intentional or accidental introduction of species, alien or new, which could cause signicant and harmful changes to the marine environment (http://www.antcrc.utas.edu.au/ opor/Treaties/unclos.html). Although the CBD and UNCLOS took effect in 1993 and 1994, respectively, the United States has not ratied either agreement. In addition, the introduction of invasive species from ballast water is being addressed at state, federal, and international levels. There is some debate as to whether the invasive species introduced through ballast water constitute a form of biological pollution, in which case the Clean Water Act would be applicable and the EPA would be required to treat invasive species in the same way as any other pollutant. 3. RISK ASSESSMENT FOR INVASIVE SPECIES Risk assessment and risk management are interacting, but functionally separate, risk analysis activities. Risk assessment characterizes the likelihood and severity of potential adverse effects of exposure to hazardous agents or activities (i.e., stressors). Risk management is the process of identifying, evaluating, selecting, and implementing actions to reduce risk.(6) There may be no sharp boundary between risk assessment and risk management in some analytic elements, e.g., the identication and evaluation of risk reduction measures. Risk managers are distinguished, however, as those with authority to make decisions and take actions to lessen or eliminate risk.(7) Risk assessment for invasive species is generally conducted to inform two classes of risk management decisions: (1) those regarding the introduction of potentially invasive nonindigenous species, their vectors, or conveyances prior to establishment (leading to decisions to authorize, prohibit, or permit activities under specied conditions), and (2) decisions regarding the allocation of scarce resources for the control of established invasive species, including rapid response to emerging threats. Because invasive species can include organisms that generate both public health and environmental concerns, risk assessments for these species provide opportunities to integrate human health and ecological risk issues. Although the EPA risk assessment

789 framework is the dominant paradigm in ecological risk assessment, it is specically intended to deal with chemical and physical stressors; its applicability to biological stressors, such as invasive species, is unclear. The OIE and IPPC risk assessment frameworks offer specic guidance for risk assessments for biological stressors. The EPA risk paradigm includes three principal elements: (1) problem formulation, (2) analysis of exposure and effects, and (3) risk characterization.(9) For invasive species, exposure analysis involves estimating the likelihood of the introduction, establishment, and/or spread of one or more potentially invasive species. Invasive species exposure analysis may consider the quantity, timing, frequency, duration, and routes of exposure as well as the numbers, species, and other characteristics (e.g., susceptibility) of the populations exposed. Effects analysis for invasive species would involve estimating the probability and severity of economic, public health, or environmental consequences of an exposure to the invasive species. As with risk assessments of other stressors, risk characterization integrates information from the problem formulation, exposure, and effects components to synthesize an overall conclusion about risk that is complete, informative, and useful for decision makers.(11) For example, Bartell and Nair (elsewhere in this Special Section) illustrate the development of exposure-response functions that integrate the ecological risk analytic components to obtain a risk characterization for the entry and establishment of a viable plant pest population under different scenarios. Complex spatial and temporal relationships present an important challenge to those responsible for assessing and managing risks associated with invasive species across multiple geographic and time zones. Furthermore, effective management of the risks posed by the invasive species requires acknowledging that: (a) although biological invasions are possible from numerous sources, nonindigenous species differ in the likelihood and consequences of establishment of spread, (b) recipient ecological communities likewise differ in their vulnerability to invasion and the values society attaches to them, (c) biological invasions differ in their susceptibility to prevention and control, and (d) scarce resources must be allocated among current and potential biological invasions through a process of balancing disparate risks, costs, and benets that are nonuniformly distributed under conditions of scientic uncertainty. In this context, risk assessment provides a deliberate, analytical

790 means for identifying how a resource could be vulnerable to a given threat and for ascertaining the probability that a threat will harm a resource with some predictable severity of consequences.(7,9) While the true value of a risk assessment can only be gauged by the extent to which it is used by risk managers to improve the quality of their management decisions, this may be difcult to discern and evaluate. Furthermore, public land managers take an active role in invasive species prevention and control. Consequently, in the context of invasive species, the authorized risk managers are commonly government ofcials. Therefore, most risk-based decisions concerning invasive species are, ultimately, public policy choices. Such choices cannot be made on the basis of science alone.(7) In formulating reasoned and balanced public policy decisions, risk managers must weigh legal, economic, administrative, social, and cultural values (e.g., equity and heritage), and other legitimate factors outside the realm of science. Ideally, however, by synthesizing and summarizing the best-available science about a potentially harmful situation, a risk assessment can provide risk managers with a dispassionate and rational basis for their decisions and actions. Thus, a risk assessment forms the link between basic and applied scientic research activities and the public policy choices of risk managers. These choices, in turn, need to be responsive to the interests and concerns of affected parties. In responding to the information needs of decision makers, however, risk assessors typically need to extrapolate beyond the available scientic data to link risk assessment endpoints to management objectives and policy goals.(6) Therefore, in order to be relevant to risk management decisions, a risk assessment must strike a balance between addressing public policy concerns and satisfying scientic criteria. Although risk assessment of invasive species has been thrust into the spotlight, relevant domestic and international guidelines and standards are at an early stage of development. Currently, the scientic discipline of risk assessment for invasive species is in its infancy. While scientists have criticized the responsible regulatory agencies for accepting staggeringly primitive theories and methods for evaluating the risks of introduced organisms, and nd the current level of risk assessment totally unacceptable, they acknowledge that it is hard to nd better approaches than those currently in use.(12) Therefore, there is a pressing need to identify, evaluate, adapt, and develop scientifically sound methods and approaches in this emerging eld.

Andersen, Hope, and Powell Traditional approaches to risk assessment of invasive species have focused primarily on problem formulation. Considerable effort has been directed to developing classication schemes to predict invasiveness (e.g., identifying species attributes that correlate with invasiveness), identifying pathways of introduction (e.g., listing host materials, infested regions, and commodities or conveyances that may harbor pests), characterizing susceptible resources (e.g., identifying attributes of recipient populations or ecological communities that correlate with vulnerability to invasion), and potential biological consequences of spread. When quantitative risk assessments have been undertaken, the assessment endpoint has generally been limited to the likelihood of entry. Consequently, there is generally a gap between risk assessment and the evaluation of potential biological and economic impacts, which is dependent on assessing the likelihood of establishment, intensity of proliferation, extent and rate of spread, and efcacy of postintroduction risk management measures.

4. SPS AGREEMENT RAISES THE BAR The gap between the information provided by current risk assessment procedures and the information needs of decision makers is particularly glaring in the context of the SPS Agreement. In effect, the SPS Agreement has raised the bar as to what qualies as an adequate risk assessment, at least for SPS measures that might be disputed as unnecessarily trade restrictive under the Agreement. Article 5.3 states: In assessing risks and determining sanitary or phytosanitary measures to achieve protection from such risks, Members must take into account the potential damage in the event of the entry, establishment, or spread of a pest or disease; the costs of control or eradication; and the relative cost-effectiveness of alternative approaches to limiting risks. In settling a dispute over Australias ban on imports of fresh and frozen salmon from Canada in order to prevent entry of 24 shborne diseases, the WTO Appellate Body established a three-pronged test for what would qualify as an adequate risk assessment under the SPS Agreement: (1) identication of the hazards (i.e., diseases) and possible biological and economic consequences of their entry or spreading, (2) evaluation of the likelihood of entry, establishment, or spreading, and (3) evaluation of the impact of SPS measures on the likelihood of entry, establishment, or spreading of the hazards.(13)

Risk Assessment for Invasive Species 5. A ROLE FOR THEORETICAL ECOLOGY In striving to meet this challenge, however, analysts and scientists need to be candid in acknowledging the limitations of the available scientic data and models to inform regulatory and natural resource management decisions concerning invasive species. This problem area is chronically confronted by a paucity of directly relevant empirical evidence. Furthermore, the demand for situation-specic data is likely to persistently outstrip supply into the foreseeable future. In addition, the complexity of biological systems (e.g., reproduction, dispersal, interspecic interactions) frequently renders verbal models and biological intuition inadequate. In this data-poor environment, it is intuitively appealing to look to the eld of theoretical ecology for insights that might be incorporated into a risk analytic framework to support policy and management decisions regarding the intentional or accidental introduction of nonindigenous species. Many theoretical results and modeling approaches that have proved useful in conservation biology (population viability analysis, gap analysis) may be able to be adapted to the specic needs of risk analysis for invasive species. The process of biological invasion can be broken into the four phases of entry, establishment, spread, and impact. The entry phase consists of the arrival (or multiple arrivals) of a nonindigenous species at one or more points of entry into a new environment. In the establishment phase, one or more of these arriving populations begins to reproduce in situ and escapes immediate danger of local extinction. In the spread phase, the species disperses from its initial site(s) of establishment and occupies available habitat (or infects susceptible hosts) within its new environment. In the impact phase, an established species persists and competes in its new geographic range. There is strong ltering of species between these phases, so that only a small fraction of species pass from the entry phase to the establishment phase, only a small proportion of those pass on to the spread phase, and a majority of species that become naturalized exert no demonstrable impact in their new range. Because successful invasion by a harmful nonindigenous species is such a rare event, this ltering process can have profound implications for our ability to detect and manage invasive species.(14,15) Applications of theoretical ecology to other environmental resource management problems suggest some potential for contributions in the context of invasive species risk assessment. In particular, many

791 of the crucial questions to be considered in studying the four phases of invasion are in some sense the inverse of some classic questions in conservation biology. For example, conservation biologists frequently ask: What aspects of a species demography might make it prone to extinction, and how might management mitigate those factors? For invasive species, management efforts are often directed at causing, rather than preventing, extinction in the new locale. A conservation biologist might ask: What inuence does the arrangement of landscape elements have on a species ability to persist? In the context of invasive species, we might want to know whether the landscape could be manipulated in such a way as to slow or halt the spread of an invader. Finally, whereas understanding the ecosystem role of an endangered species might help us to manage for that species survival, understanding the ecosystem impacts of an invasive species may suggest ways to prevent or mitigate those impacts. Of these four phases, entry has been the most convenient focus of risk assessment efforts, through a process of documenting potential invaders that may be brought in as hitchhikers with some imported commodity.(16,17) Due to the prevalent effects of demographic and environmental stochasticity on small populations, there is an especially strong ltering of species at this stage. This ltering implies that it is easier to identify potential invaders among species in the establishment phase rather than at the entry phase.(14) The fact that it is easier to assess the invasive potential of established species, however, poses severe problems for predictive risk assessment and risk management due to the difculty of eradicating or controlling nonindigenous populations after establishment. Applicable ecological theory is considerably more well developed for the remaining three phases of the species invasion process. There is a welldeveloped body of theory on extinction, most of which is applicable to establishment,(1821) as well as some direct applications of theory to the problem of establishment.(22) Much of this theory has found direct applications already in the eld of conservation biology. Due to the recent advances in our ability to analyze integrodifference-equation models, there is also a growing body of theory applicable to the spread phase.(23,24) Finally, ecologists have amassed a great deal of empirical information on the ecological impacts of invasive species.(5,15) We may think of the ecological impact of an invasive species as including three components: the invaders geographic and

792 habitat range, its abundance, and its per-capita or perunit-biomass effect on the ecosystem.(5) A few potentially useful predictions and guidelines have resulted from the study of biological invasions. These predictions fall into two primary categories. On the one hand, there has been considerable research on biological characteristics of species that are most likely to become invasive pests.(2529) As Smith et al.(14) point out, however, the accuracy of such predictions (the proportion of a group of classied pest species that would be correctly identied as pests) needs to be distinguished from their reliability (the rate of false positives and false negatives). On the other hand, there has been somewhat less research on types of habitats that are most susceptible to invasion.(30) Predicting susceptible locales for the future invasions has proven even more problematic than identifying general attributes of future invasive species.(15) 6. DISCUSSION In general, the study of invasive species is a eld with a great need for synthesis, with great opportunities for theoretical development, and for direct contribution of those developments to management methodology. Disagreements over interpretation of available data(31,32) may result from lack of recognition that different ecological processes may inuence different phases of the invasion process, and that different traits of both species and habitats may determine success at different phases. As Parker et al.(5) observe, there can be a considerable disagreement over the magnitude of ecological impacts caused by even notorious biological invasions, such as that of Cryphonectria parasitica, the blight fungus that devastated the American chestnut (Castanea dentata) populations that were formerly a dominant component of the U.S. eastern deciduous forest. Similarly, purple loosestrife (Lythrum salicaria) is generally regarded as an aggressive invader that displaces native wetlands vegetation and may adversely impact waterfowl habitat by forming dense, nearly monotypic stands; however, Hager and McCoy(33) found little scientic evidence that the plant has deleterious effects on North American wetlands. The use of different metrics (e.g., changes in ecosystem function versus changes in species composition) can lead to different conclusions about the importance, magnitude, or even direction of the ecological impacts of introduced species. In addition, seemingly narrow disagreements over scientic interpretation may serve as proxies for

Andersen, Hope, and Powell broader disagreements over policy and values. That is, although the terms of the debate may be scientic, the root of the dispute may be social. Therefore, progress in risk assessment for invasive species will depend on clarication of terminology, adherence to agreed-upon denitions of concepts, synthesis of empirical results, and induction of theoretical principles from those syntheses that leads to a greater understanding of the ecology of biological invasions. All this discussion illustrates the need for clear agreement on appropriate risk assessment endpoints, ensuring clear and defensible communication and implementation of risk assessments. 7. PAPERS IN THIS SPECIAL SECTION To begin addressing some of the many challenges facing the eld of risk assessment for invasive species, on October 2123, 2001, New Mexico State University convened a joint workshop of the Society for Risk Analysis Ecological Risk Assessment Specialty Group and the Ecological Society of America Theoretical Ecology Section conducted under a cooperative agreement between the University and the U.S. Department of Agriculture Ofce of Risk Assessment and Cost-Benet Analysis. This special section of Risk Analysis is based upon several papers originally developed for and presented at the workshop. With applies grid-based neutral landscape models to explore the impact of landscape fragmentation on the risk of invasive spread. Neubert presents the use of integrodifference-equation (IDE) models, originally formulated to describe the advantageous alleles in genetic studies, to project rates of spread for invading species. Bartell et al. present a quantitative framework for evaluating reductions in the risk of plant pest introduction and establishment afforded by treating solid wood packing material before its import into the United States. Landis highlights the importance of incorporating spatial and temporal relationships within a landscape for ecological risk assessment of invasive species. Maguire suggests how a multi-attribute utility analysis may contribute to invasive species management. Marvier et al. discuss the role that cost-benet analysis plays in framing the questions addressed by risk assessment of invasive species and highlight aspects of ecological theory that could produce pragmatic guidance for efcient control of invasive species. Sharov provides an example of the integration of biological and economic information to optimize management actionseradication, suppression, or doing nothingalong the front of an expanding invasive

Risk Assessment for Invasive Species population. It is our hope that these papers will provide guidance for defensible risk analyses, and impetus for further research and development of risk analysis tools based on theoretical ecology. REFERENCES
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