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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 devel-
oping 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 scientific 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 unjustifiable
technical barriers to trade. Currently, however, the field of risk assessment for invasive species
is in its infancy. Therefore, there is a pressing need to formulate scientifically sound methods
and approaches in this emerging field, while acknowledging that the demand for situation-
specific 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 Eco-
logical Society of America Theoretical Ecology Section convened a joint workshop to provide
independent scientific 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 firmly rooted in sound scientific principles.

KEY WORDS: Invasive species; risk assessment; theoretical ecology

1. BACKGROUND tal and therefore invasive. In many cases, the classi-


fication of nonindigenous species is complicated by
The entry, establishment, and spread of non-
offsetting benefits from damages.
indigenous species in new environments can cause
Invasive species such as the zebra mussel (Dreis-
major economic damage, irreversible ecological
sena polymorpha), which can clog water pipes for
changes, and significant public health impacts. While
electric power plants and municipal and irrigation
many nonindigenous species provide benefits in their
water supplies, cause tangible economic damages. In-
new environment (e.g., the major crop plants), or are
vasive species also may diminish the provision of non-
considered benign, others are regarded as detrimen-
market environmental goods and services (e.g., water
1 Department of Fishery and Wildlife Sciences, New Mexico State
quality). Nonindigenous invasive species can impact
University, Las Cruces, NM 88003-003, USA. native ecological communities directly (through pre-
2 Oregon Dept of Environmental Quality, Portland, OR 97215- dation, grazing, parasitism, infection, competition, or
2654, USA. hybridization). Their impacts also may be brought
3 USDA Office of Risk Assessment and Cost Benefit Analysis,
about indirectly through modification of ecosystem
Washington, DC 20250, USA.
∗ Address correspondence to Mark C. Andersen, Department of functions (e.g., by altering fire regimes, hydrology, nu-
Fishery and Wildlife Sciences, New Mexico State University, trient cycles, and energy flows). The introduction of
Las Cruces, NM 88003-003, USA; manderse@nmsu.edu. nonindigenous infectious agents (e.g., West Nile virus)

787 0272-4332/04/0100-0787$22.00/1 
C 2004 Society for Risk Analysis
788 Andersen, Hope, and Powell

and/or exotic disease vectors present risks to public invasive species issues and is co-chaired by the Secre-
health and to the health of domestic and wild animal taries of Agriculture, Interior, and Commerce. E.O.
and plant populations. 13112 requires a science-based process to evaluate
Taken alone, the estimated economic damages risks associated with the introduction and spread of in-
resulting from individual invasive species can be vasive species, and a coordinated and systematic risk-
significant. For example, since its introduction, the un- based process to identify, monitor, and interdict path-
palatable weed, leafy spurge (Euphorbia esula), has ways that may be involved in the introduction of in-
spread to more than 5 million acres of rangeland in the vasive species. The NISC 2001 National Management
northern Great Plains, causing estimated production Plan calls for development of a risk analysis system
losses, control expenses, and other economic damages for nonnative species by 2003.(1)
in excess of $100 million per year. The total cost of the The issue of invasive species has been elevated
eradication program for citrus canker (Xanthomonas onto the international trade and environmental pol-
campestris pv. citri) is expected to exceed $200 million. icy agendas through a variety of international agree-
The U.S. Department of Agriculture 2001 fiscal year ments and by conspicuous incursions of nonindige-
budget for invasive species activities alone exceeded nous pests. An obvious example of such a pest is
$580 million. Recent studies that have attempted to the Asian longhorned beetle (Anoplophora glabri-
estimate the total national impact of invasive species pennis), which has infested hardwood trees in U.S.
also suggest that the overall magnitude of annual eco- metropolitan areas. Under the World Trade Organi-
nomic change exceeds the federally-defined threshold zation (WTO) Sanitary and Phytosanitary Agreement
of $100 million per year for “major” economic im- (SPS Agreement), members of the international trad-
pacts.(1–4) ing community have agreed to adhere to the disci-
Invasive species may cause irreversible changes pline of scientific risk assessment. This is to ensure
to ecological communities by altering the composition that the SPS measures are applied only to the extent
and abundance of native species, in some cases, to the required to protect human, animal, and plant health,
point of extinction. The Office of Technology Assess- and do not constitute arbitrary or unjustifiable tech-
ment(2) provides a discussion of the evidence impli- nical barriers to trade (http://www.wto.org/english/
cating invasive species in the extinction or endanger- tratop e/sps e/sps e.htm). The SPS Agreement rec-
ment of species native to the United States. One of ognizes the World Organization for Animal Health
the few accepted generalizations about the ecological (Office International des Epizooties, or OIE) and
effects of biological invasions is that the greatest im- the international and regional organizations operat-
pacts occur when a nonindigenous species performs ing within the framework of the International Plant
an entirely novel function in the recipient community. Protection Convention (IPPC) as the international
Examples include invasions of oceanic island commu- standard-setting bodies for animal health and phy-
nities by mammalian predators and the invasion of tosanitary measures, respectively. The scope of OIE
nitrogen-fixing plants in regions with nitrogen-poor guidelines for terrestrial and aquatic animal health
soils.(5) In addition to many of the problems beset- risk assessment includes the potential public health
ting economic impact assessments, ecological impact and environmental consequences of pathogenic
assessment of invasive species is further hindered by agents (http://www.oie.int/eng/en index.htm). The
the lack of a common currency for measuring and IPPC Interim Commission on Phytosanitary Mea-
expressing changes, by uncertainty or disagreement sures recently initiated efforts to develop standards
about what constitutes an adverse ecological impact, for conducting plant pest risk analysis for environ-
and by the difficulties of predicting the nature and mental hazards, to explicitly address risks to nonagro-
amounts of impacts. nomic ecosystems, where plant pests include plants,
animals, or pathogenic agents directly or indirectly
injurious to plants or plant products (http://www.fao.
2. INVASIVE SPECIES ON THE org/WAICENT/FaoInfo/Agricult/AGP/AGPP/PQ).
POLICY AGENDA Invasive species issues are also being elevated
The National Invasive Species Council (NISC) onto the international agenda via the Convention
coordinates the U.S. domestic effort to manage risks on Biological Diversity (CBD), which urges coun-
associated with invasive species. The NISC, estab- tries to prevent the introduction of and to control or
lished in 1999 by Executive Order 13112, consists of eradicate nonnative species that threaten ecosystems,
eight federal departments with leadership roles for habitats, or species (http://www.biodiv.org). The CBD
Risk Assessment for Invasive Species 789

Biosafety Protocol (known familiarly as the Carte- framework is the dominant paradigm in ecological
gena Protocol) requires decisions regarding the inter- risk assessment, it is specifically intended to deal with
national movement of living modified organisms to chemical and physical stressors; its applicability to bi-
be subject to risk assessment (http://www.biodiv.org/ ological stressors, such as invasive species, is unclear.
biosafety). Article 196 of the United Nations Conven- The OIE and IPPC risk assessment frameworks offer
tion on the Law of the Sea (UNCLOS) calls for mea- specific guidance for risk assessments for biological
sures to prevent, reduce, and control the intentional or stressors.
accidental introduction of species, alien or new, which The EPA risk paradigm includes three principal
could cause significant and harmful changes to the elements: (1) problem formulation, (2) analysis of ex-
marine environment (http://www.antcrc.utas.edu.au/ posure and effects, and (3) risk characterization.(9)
opor/Treaties/unclos.html). Although the CBD and For invasive species, exposure analysis involves es-
UNCLOS took effect in 1993 and 1994, respectively, timating the likelihood of the introduction, establish-
the United States has not ratified either agreement. ment, and/or spread of one or more potentially inva-
In addition, the introduction of invasive species sive species. Invasive species exposure analysis may
from ballast water is being addressed at state, federal, consider the quantity, timing, frequency, duration, and
and international levels. There is some debate as to routes of exposure as well as the numbers, species, and
whether the invasive species introduced through bal- other characteristics (e.g., susceptibility) of the popu-
last water constitute a form of “biological pollution,” lations exposed. Effects analysis for invasive species
in which case the Clean Water Act would be applica- would involve estimating the probability and sever-
ble and the EPA would be required to treat invasive ity of economic, public health, or environmental con-
species in the same way as any other pollutant. sequences of an “exposure” to the invasive species.
As with risk assessments of other stressors, risk char-
acterization integrates information from the prob-
3. RISK ASSESSMENT FOR
lem formulation, exposure, and effects components to
INVASIVE SPECIES
synthesize an overall conclusion about risk that is
Risk assessment and risk management are inter- complete, informative, and useful for decision mak-
acting, but functionally separate, risk analysis activi- ers.(11) For example, Bartell and Nair (elsewhere in
ties. Risk assessment characterizes the likelihood and this Special Section) illustrate the development of
severity of potential adverse effects of exposure to “exposure-response” functions that integrate the eco-
hazardous agents or activities (i.e., stressors). Risk logical risk analytic components to obtain a risk
management is the process of identifying, evaluating, characterization for the entry and establishment
selecting, and implementing actions to reduce risk.(6) of a viable plant pest population under different
There may be no sharp boundary between risk assess- scenarios.
ment and risk management in some analytic elements, Complex spatial and temporal relationships
e.g., the identification and evaluation of risk reduction present an important challenge to those responsible
measures. Risk managers are distinguished, however, for assessing and managing risks associated with in-
as those with authority to make decisions and take vasive species across multiple geographic and time
actions to lessen or eliminate risk.(7) Risk assessment zones. Furthermore, effective management of the
for invasive species is generally conducted to inform risks posed by the invasive species requires acknowl-
two classes of risk management decisions: (1) those re- edging that: (a) although biological invasions are pos-
garding the introduction of potentially invasive non- sible from numerous sources, nonindigenous species
indigenous species, their vectors, or conveyances prior differ in the likelihood and consequences of estab-
to establishment (leading to decisions to authorize, lishment of spread, (b) recipient ecological commu-
prohibit, or permit activities under specified condi- nities likewise differ in their vulnerability to invasion
tions), and (2) decisions regarding the allocation of and the values society attaches to them, (c) biologi-
scarce resources for the control of established invasive cal invasions differ in their susceptibility to preven-
species, including rapid response to emerging threats. tion and control, and (d) scarce resources must be
Because invasive species can include organisms allocated among current and potential biological in-
that generate both public health and environmental vasions through a process of balancing disparate risks,
concerns, risk assessments for these species provide costs, and benefits that are nonuniformly distributed
opportunities to integrate human health and ecolog- under conditions of scientific uncertainty. In this con-
ical risk issues. Although the EPA risk assessment text, risk assessment provides a deliberate, analytical
790 Andersen, Hope, and Powell

means for identifying how a resource could be vulner- Traditional approaches to risk assessment of in-
able to a given threat and for ascertaining the prob- vasive species have focused primarily on problem
ability that a threat will harm a resource with some formulation. Considerable effort has been directed
predictable severity of consequences.(7,9) While the to developing classification schemes to predict in-
true value of a risk assessment can only be gauged by vasiveness (e.g., identifying species attributes that
the extent to which it is used by risk managers to im- correlate with invasiveness), identifying pathways of
prove the quality of their management decisions, this introduction (e.g., listing host materials, infested re-
may be difficult to discern and evaluate. gions, and commodities or conveyances that may har-
Furthermore, public land managers take an active bor pests), characterizing susceptible resources (e.g.,
role in invasive species prevention and control. Con- identifying attributes of recipient populations or eco-
sequently, in the context of invasive species, the autho- logical communities that correlate with vulnerability
rized risk managers are commonly government offi- to invasion), and potential biological consequences
cials. Therefore, most risk-based decisions concerning of spread. When quantitative risk assessments have
invasive species are, ultimately, public policy choices. been undertaken, the assessment endpoint has gen-
Such choices cannot be made on the basis of science erally been limited to the likelihood of entry. Conse-
alone.(7) In formulating reasoned and balanced pub- quently, there is generally a gap between risk assess-
lic policy decisions, risk managers must weigh legal, ment and the evaluation of potential biological and
economic, administrative, social, and cultural values economic impacts, which is dependent on assessing
(e.g., equity and heritage), and other legitimate fac- the likelihood of establishment, intensity of prolifer-
tors outside the realm of science. Ideally, however, ation, extent and rate of spread, and efficacy of post-
by synthesizing and summarizing the best-available introduction risk management measures.
science about a potentially harmful situation, a risk
assessment can provide risk managers with a dispas-
sionate and rational basis for their decisions and ac-
4. SPS AGREEMENT RAISES THE BAR
tions. Thus, a risk assessment forms the link between
basic and applied scientific research activities and the The gap between the information provided by
public policy choices of risk managers. These choices, current risk assessment procedures and the informa-
in turn, need to be responsive to the interests and tion needs of decision makers is particularly glaring in
concerns of affected parties. In responding to the in- the context of the SPS Agreement. In effect, the SPS
formation needs of decision makers, however, risk as- Agreement has raised the bar as to what qualifies as
sessors typically need to extrapolate beyond the avail- an adequate risk assessment, at least for SPS mea-
able scientific data to link risk assessment endpoints sures that might be disputed as unnecessarily trade
to management objectives and policy goals.(6) There- restrictive under the Agreement. Article 5.3 states:
fore, in order to be relevant to risk management deci- “In assessing risks and determining sanitary or phy-
sions, a risk assessment must strike a balance between tosanitary measures to achieve protection from such
addressing public policy concerns and satisfying sci- risks, Members must take into account the potential
entific criteria. damage in the event of the entry, establishment, or
Although risk assessment of invasive species has spread of a pest or disease; the costs of control or
been thrust into the spotlight, relevant domestic and eradication; and the relative cost-effectiveness of al-
international guidelines and standards are at an early ternative approaches to limiting risks.” In settling a
stage of development. Currently, the scientific disci- dispute over Australia’s ban on imports of fresh and
pline of risk assessment for invasive species is in its in- frozen salmon from Canada in order to prevent entry
fancy. While scientists have criticized the responsible of 24 fishborne diseases, the WTO Appellate Body es-
regulatory agencies for accepting “staggeringly prim- tablished a three-pronged test for what would qualify
itive” theories and methods for evaluating the risks as an adequate risk assessment under the SPS Agree-
of introduced organisms, and find the current level of ment: (1) identification of the hazards (i.e., diseases)
risk assessment “totally unacceptable,” they acknowl- and possible biological and economic consequences
edge that “it is hard to find better approaches” than of their entry or spreading, (2) evaluation of the
those currently in use.(12) Therefore, there is a pressing likelihood of entry, establishment, or spreading, and
need to identify, evaluate, adapt, and develop scientif- (3) evaluation of the impact of SPS measures on the
ically sound methods and approaches in this emerging likelihood of entry, establishment, or spreading of the
field. hazards.(13)
Risk Assessment for Invasive Species 791

5. A ROLE FOR THEORETICAL ECOLOGY of the crucial questions to be considered in studying


the four phases of invasion are in some sense the in-
In striving to meet this challenge, however, anal- verse of some classic questions in conservation biol-
ysts and scientists need to be candid in acknowledging ogy. For example, conservation biologists frequently
the limitations of the available scientific data and ask: “What aspects of a species’ demography might
models to inform regulatory and natural resource make it prone to extinction, and how might manage-
management decisions concerning invasive species. ment mitigate those factors?” For invasive species,
This problem area is chronically confronted by a management efforts are often directed at causing,
paucity of directly relevant empirical evidence. Fur- rather than preventing, extinction in the new locale.
thermore, the demand for situation-specific data is A conservation biologist might ask: “What influence
likely to persistently outstrip supply into the foresee- does the arrangement of landscape elements have on
able future. In addition, the complexity of biological a species’ ability to persist?” In the context of inva-
systems (e.g., reproduction, dispersal, interspecific in- sive species, we might want to know whether the land-
teractions) frequently renders verbal models and bi- scape could be manipulated in such a way as to slow or
ological intuition inadequate. In this data-poor en- halt the spread of an invader. Finally, whereas under-
vironment, it is intuitively appealing to look to the standing the ecosystem role of an endangered species
field of theoretical ecology for insights that might be might help us to manage for that species’ survival,
incorporated into a risk analytic framework to sup- understanding the ecosystem impacts of an invasive
port policy and management decisions regarding the species may suggest ways to prevent or mitigate those
intentional or accidental introduction of nonindige- impacts.
nous species. Many theoretical results and modeling Of these four phases, entry has been the most
approaches that have proved useful in conservation convenient focus of risk assessment efforts, through a
biology (population viability analysis, gap analysis) process of documenting potential invaders that may
may be able to be adapted to the specific needs of risk be brought in as “hitchhikers” with some imported
analysis for invasive species. commodity.(16,17) Due to the prevalent effects of de-
The process of biological invasion can be broken mographic and environmental stochasticity on small
into the four phases of entry, establishment, spread, populations, there is an especially strong filtering of
and impact. The entry phase consists of the arrival (or species at this stage. This filtering implies that it is
multiple arrivals) of a nonindigenous species at one or easier to identify potential invaders among species
more points of entry into a new environment. In the in the establishment phase rather than at the entry
establishment phase, one or more of these arriving phase.(14) The fact that it is easier to assess the inva-
populations begins to reproduce in situ and escapes sive potential of established species, however, poses
immediate danger of local extinction. In the spread severe problems for predictive risk assessment and
phase, the species disperses from its initial site(s) of risk management due to the difficulty of eradicat-
establishment and occupies available habitat (or in- ing or controlling nonindigenous populations after
fects susceptible hosts) within its new environment. In establishment.
the impact phase, an established species persists and Applicable ecological theory is considerably
competes in its new geographic range. There is strong more well developed for the remaining three phases
filtering of species between these phases, so that only of the species invasion process. There is a well-
a small fraction of species pass from the entry phase developed body of theory on extinction, most of which
to the establishment phase, only a small proportion is applicable to establishment,(18–21) as well as some
of those pass on to the spread phase, and a majority direct applications of theory to the problem of es-
of species that become naturalized exert no demon- tablishment.(22) Much of this theory has found direct
strable impact in their new range. Because successful applications already in the field of conservation biol-
invasion by a harmful nonindigenous species is such ogy. Due to the recent advances in our ability to ana-
a rare event, this filtering process can have profound lyze integrodifference-equation models, there is also
implications for our ability to detect and manage in- a growing body of theory applicable to the spread
vasive species.(14,15) phase.(23,24) Finally, ecologists have amassed a great
Applications of theoretical ecology to other en- deal of empirical information on the ecological im-
vironmental resource management problems suggest pacts of invasive species.(5,15) We may think of the
some potential for contributions in the context of in- ecological impact of an invasive species as includ-
vasive species risk assessment. In particular, many ing three components: the invader’s geographic and
792 Andersen, Hope, and Powell

habitat range, its abundance, and its per-capita or per- broader disagreements over policy and values. That
unit-biomass effect on the ecosystem.(5) is, although the terms of the debate may be scien-
A few potentially useful predictions and guide- tific, the root of the dispute may be social. Therefore,
lines have resulted from the study of biological progress in risk assessment for invasive species will
invasions. These predictions fall into two primary depend on clarification of terminology, adherence to
categories. On the one hand, there has been consider- agreed-upon definitions of concepts, synthesis of em-
able research on biological characteristics of species pirical results, and induction of theoretical principles
that are most likely to become invasive pests.(25–29) from those syntheses that leads to a greater under-
As Smith et al.(14) point out, however, the accuracy of standing of the ecology of biological invasions. All this
such predictions (the proportion of a group of clas- discussion illustrates the need for clear agreement on
sified pest species that would be correctly identified appropriate risk assessment endpoints, ensuring clear
as pests) needs to be distinguished from their relia- and defensible communication and implementation
bility (the rate of false positives and false negatives). of risk assessments.
On the other hand, there has been somewhat less re-
search on types of habitats that are most susceptible
7. PAPERS IN THIS SPECIAL SECTION
to invasion.(30) Predicting susceptible locales for the
future invasions has proven even more problematic To begin addressing some of the many challenges
than identifying general attributes of future invasive facing the field of risk assessment for invasive species,
species.(15) on October 21–23, 2001, New Mexico State Univer-
sity convened a joint workshop of the Society for
Risk Analysis Ecological Risk Assessment Specialty
6. DISCUSSION
Group and the Ecological Society of America Theo-
In general, the study of invasive species is a field retical Ecology Section conducted under a coopera-
with a great need for synthesis, with great oppor- tive agreement between the University and the U.S.
tunities for theoretical development, and for direct Department of Agriculture Office of Risk Assess-
contribution of those developments to management ment and Cost-Benefit Analysis. This special section
methodology. Disagreements over interpretation of of Risk Analysis is based upon several papers origi-
available data(31,32) may result from lack of recogni- nally developed for and presented at the workshop.
tion that different ecological processes may influence With applies grid-based neutral landscape models to
different phases of the invasion process, and that dif- explore the impact of landscape fragmentation on the
ferent traits of both species and habitats may deter- risk of invasive spread. Neubert presents the use of
mine success at different phases. As Parker et al.(5) integrodifference-equation (IDE) models, originally
observe, there can be a considerable disagreement formulated to describe the advantageous alleles in ge-
over the magnitude of ecological impacts caused by netic studies, to project rates of spread for invading
even notorious biological invasions, such as that of species. Bartell et al. present a quantitative frame-
Cryphonectria parasitica, the blight fungus that dev- work for evaluating reductions in the risk of plant pest
astated the American chestnut (Castanea dentata) introduction and establishment afforded by treating
populations that were formerly a dominant compo- solid wood packing material before its import into the
nent of the U.S. eastern deciduous forest. Similarly, United States. Landis highlights the importance of in-
purple loosestrife (Lythrum salicaria) is generally re- corporating spatial and temporal relationships within
garded as an aggressive invader that displaces native a landscape for ecological risk assessment of invasive
wetlands vegetation and may adversely impact wa- species. Maguire suggests how a multi-attribute utility
terfowl habitat by forming dense, nearly monotypic analysis may contribute to invasive species manage-
stands; however, Hager and McCoy(33) found little sci- ment. Marvier et al. discuss the role that cost-benefit
entific evidence that the plant has deleterious effects analysis plays in framing the questions addressed
on North American wetlands. The use of different by risk assessment of invasive species and highlight
metrics (e.g., changes in ecosystem function versus aspects of ecological theory that could produce prag-
changes in species composition) can lead to differ- matic guidance for efficient control of invasive species.
ent conclusions about the importance, magnitude, or Sharov provides an example of the integration of bi-
even direction of the ecological impacts of introduced ological and economic information to optimize man-
species. In addition, seemingly narrow disagreements agement actions—eradication, suppression, or doing
over scientific interpretation may serve as proxies for nothing—along the front of an expanding invasive
Risk Assessment for Invasive Species 793

population. It is our hope that these papers will 15. Mack, R. N., Simberloff, D., Lonsdale, W. M., Evans, H.,
provide guidance for defensible risk analyses, and Clout, M., & Bazzaz, F. (2000). Biotic invasions: Causes,
epidemiology, global consequences, and control. Issues in
impetus for further research and development of risk Ecology, 5.
analysis tools based on theoretical ecology. 16. Tkacz, B. M., Burdsall, Jr., H. H., DeNitto, G. A., et al. (1998).
Report No. Gen. Tech. Rep. FPL-GTR-104. Madison, WI: U.S.
Department of Agriculture, Forest Service, Forest Products
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