Invasive Species, Environmental Change and Management, and ...faculty.washington.edu/wgold/BES301/invasive... · EG35CH02-Pysek ARI 18 September 2010 6:55 Invasive Species, Environmental

EG35CH02-Pysek ARI 18 September 2010 6:55

Invasive Species,Environmental Change andManagement, and HealthPetr Pysek1,2 and David M. Richardson3

1Institute of Botany, Academy of Sciences of the Czech Republic, CZ-252 43 Pruhonice,Czech Republic; email: [email protected] of Ecology, Faculty of Science, Charles University, CZ-128 01 Praha 2,Czech Republic3Centre for Invasion Biology, Department of Botany and Zoology, Stellenbosch University,Matieland 7602, South Africa; email: [email protected]

Annu. Rev. Environ. Resour. 2010. 35:25–55

First published online as a Review in Advance onJune 2, 2010

The Annual Review of Environment and Resourcesis online at environ.annualreviews.org

This article’s doi:10.1146/annurev-environ-033009-095548

Copyright c© 2010 by Annual Reviews.All rights reserved

1543-5938/10/1121-0025$20.00

Key Words

biological invasions, early detection, ecological and economic impacts,novel ecosystems, pathway and vector management, rapid response,risk assessment

Abstract

Invasive species are a major element of global change and are con-tributing to biodiversity loss, ecosystem degradation, and impairmentof ecosystem services worldwide. Research is shedding new light on theecological and economic consequences of invasions. New approachesare emerging for describing and evaluating impacts of invasive species,and for translating these impacts into monetary terms. The harmful ef-fects of invasions are now widely recognized, and multiscale programsare in place in many parts of the world to reduce current and futureimpacts. There has been an upsurge in scientific research aimed at guid-ing management interventions. Among the activities that are receivingthe most attention and that have the most promise for reducing prob-lems are risk assessment, pathway and vector management, early detec-tion, rapid response, and new approaches to mitigation and restoration.Screening protocols to reduce new introductions are becoming moreaccurate and have been shown cost-effective.

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Contents

INTRODUCTION . . . . . . . . . . . . . . . . . . 26Why Invasions Happen: Key

Concepts . . . . . . . . . . . . . . . . . . . . . . . 27Stages of Invasions: Which Species

Should Management Address . . . . 28IMPACT OF INVASIVE SPECIES

AND ENVIRONMENTALCHANGE . . . . . . . . . . . . . . . . . . . . . . . . 30Ecological Consequences

of Biological Invasions . . . . . . . . . . 30Ecosystem Services

and Human Health . . . . . . . . . . . . . 33Comparing Ecological

and Economic Impacts . . . . . . . . . . 34Impacts in Monetary Terms . . . . . . . . 35Limitations of Measuring Impact . . . 38

MANAGEMENT OFBIOLOGICAL INVASIONS . . . . . . 40Risk Assessment . . . . . . . . . . . . . . . . . . . 40Pathway and Vector Management . . 42Early Detection and Rapid

Response . . . . . . . . . . . . . . . . . . . . . . . 43Eradication . . . . . . . . . . . . . . . . . . . . . . . . 44Mitigation and Restoration . . . . . . . . . 45Novel Ecosystems: Refocusing

on Management Targets . . . . . . . . 46CONCLUSIONS . . . . . . . . . . . . . . . . . . . . 46

INTRODUCTIONThe extent of biological invasions has increasedrapidly over the past half century (1–3). Alongwith other drivers of ecosystem degradationsuch as habitat change and exploitation, envi-ronmental pollution, climate change, and as-sociated effects, including the loss of keystonespecies, loss of pollinators and altered ecosys-tem functioning (Figure 1, see color insert), bi-ological invasions contribute to the decline ofbiodiversity worldwide (2, 4). With increasingawareness of the complexity of problems withinvasive species, invasion ecology has taken itsplace at the table with other disciplines in en-vironmental management that have themselvesevolved in response to challenges in biodiver-sity conservation (Figure 1). Invasion ecology

has exploded to embrace and borrow insights,methods, and approaches from biogeography,conservation biology, epidemiology, humanhistory, population ecology, and many otherdomains. This reflects the massive increase inthe number and extent of invasive species andinvasion events worldwide, as well as the radicalescalation of the implications of invasions. Veryfew ecosystems anywhere in the world are freeof introduced species, and an increasing pro-portion of biomes, ecosystems, and habitats arebecoming dominated by introduced species.

Negative effects on biodiversity are gener-ally the main concern associated with biologicalinvasions, but invasions also have serious im-plications for human well-being. Most humansrely on alien species for the bulk of theirrequirements for food and other basic require-ments, although there is increasing realizationof the importance of conserving natural capitalto ensure the sustainable provision of crucialecosystems services. The Millennium Ecosys-tem Assessment (2) recognized biological inva-sions as one of the five main causes of declinesof biodiversity, which translates into reducedecosystem services worldwide. The rank ofinvasions as a threat varies across biomes andis most serious in coastal areas, inland waters,and Mediterranean-climate zones as well as onislands. Invasions also have rapidly increasingimpacts in biomes that are not yet seriously af-fected, e.g., dryland and forest zones. Economiccosts to society of harmful invasive species in-volve those associated with losses of biodiversityand impaired ecosystem services, as well as thecosts of controlling invasive species and reduc-ing and mitigating their impacts. Synergisticinteractions between invasive species and otherelements of global change make it difficult toassign a rank to specific causes of biodiversitydecline, but invasions are a fundamental driverof ecosystem degradation in many parts of theworld. Invasion ecology, and the managementof invasions, now grapples with the extremecomplexity implicit in gaining a predictive un-derstanding of the spatial dynamics of invadingspecies, the range of interactions betweennonnative species and natives, the effects of

26 Pysek · Richardson

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invading species on biodiversity and ecosystemfunctioning, and the full range of human valuesassociated with decisions on whether and, if so,how to manage introduced species.

Our review deals with invasive species as acomponent of global change and focuses on is-sues dealing with introduced species that in-creasingly demand management intervention.We first provide a primer on key concepts andterminology, then review the impact of biolog-ical invasions in the context of ongoing envi-ronmental change, and, finally, review recentprogress in the management of invasions anddiscuss what can be done to mitigate this prob-lem. We hope that the article points researchersto gaps in our knowledge and to important av-enues for research, helps practitioners in thefield to become aware of new tools and meth-ods that are available for improved manage-ment of biological invasions, and contributes toimproved communication and interaction be-tween researchers and managers.

Why Invasions Happen: Key Concepts

Much work has been done in recent decadeson every conceivable facet of invasion ecology(5–7), and our understanding of why invasionshappen has improved substantially. Three bigquestions underpin most work in invasion ecol-ogy: Which species invade; which habitats areinvaded; and how can we manage invasions?Some organizing and unifying themes in thefield are organism focused and relate to speciesinvasiveness; others are ecosystem centered anddeal with determinants of the invasibility ofcommunities, habitats, and regions. Recently,some theories have taken an overarching ap-proach to plant invasions by integrating theconcepts of species invasiveness and commu-nity invasibility (5).

The process of invasion can be concep-tualized with reference to the naturalization-invasion continuum (Figure 2a, see colorinsert), which posits that an alien species needsto overcome a sequence of barriers to becomenaturalized or invasive (5, 8). A species isintroduced from a region where it is native

by means of human action via various path-ways, including both deliberate introductionand release into the wild, and unintentionalintroduction (9). Only a fraction of introducedspecies successfully establishes or invades in thenew region (Figure 2b) (10). Whether or notthey succeed depends on how their biologicaltraits equip them for dealing with the rigors ofthe new environment, whether they are able toreproduce, disperse, and successfully competewith resident biota in local communities (11,12), but also on the habitat and climate matchbetween the native and invaded region and onthe invasibility of recipient communities. Traitscontributing to the success of taxa as invasivealiens are not universal and need to be relatedto the features of the invaded community,geographical conditions, and a set of externalfactors, including propagule pressure (5). Inthe new region, synergistic interactions mayoccur among invaders that accelerate invasionsand/or amplify their effects on native commu-nities (Figure 2e) (13). Stochastic effects, whichdepend on initial inoculum size, residence time(i.e., the time since the introduction of a taxonto a new area), chance events, and propagulepressure (defined as the number of introduc-tion events) (14), and their spatial distributioncodetermine whether a species becomes inva-sive. A key generalization is that the probabilityof invasion increases with residence time.

An introduced species invading a new regionmust either possess sufficiently high levels ofphysiological tolerance and plasticity, or it mustundergo genetic differentiation to achieve therequired levels of fitness; these options are notmutually exclusive. Available evidence suggeststhat some invaders are “born” (released fromfitness constraints), that some are “made” (theyevolve invasiveness after colonization), andthat the relative importance of ecological andevolutionary forces is unique to each invasionepisode. It has been shown that evolution, asa potential explanation for invasion success,can be rapid enough to be relevant over thetimescales at which invasions occur. Hybridiza-tion is an important mechanism of evolution ofinvasive plant species, and many widespread,

www.annualreviews.org • Management of Biological Invasions 27

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successful plant invaders are recently formedallopolyploid hybrids (15). Escape from naturalenemies is another important mechanismleading to evolution of invasiveness; plantsintroduced into an environment that lackssuch enemies may experience selection towardallocating less energy to defense and more togrowth and reproduction (16). Enemy releaseis greater in plant species adapted, in theirnative range, to resource-rich environments,and these species are likely to become invadersbecause of their capability for fast growth.Therefore, enemy release and resource-useefficiency act synergistically (17).

The ability of an alien species to overcomevarious barriers in the new environment is af-fected, positively or negatively, by the presenceof other species, native or alien, already resi-dent in the area. Such interactions may counteror even override any inherent biotic resistance.Some communities and/or ecosystems are moreinvasible than others; their inherent invasibilitydepends on the level of resources available atthe time of invasion, which is closely linked tothe disturbance level (18), but also on the pres-ence of herbivores, pathogens, and predatorsthat can act as a constraint to the establishmentof new species. The key factor is the rate of sur-vival of alien species introduced into the com-munity (19). The extent to which a communityis invaded (level of invasion) is an interplay of itsinherent invasibility and the propagule pressureto which it is exposed (5, 19, 20). If propagulepressure is high enough, even moderately resis-tant communities can become invaded (21).

Last but not least, cultural influence, re-gional history (22), as well as economic and so-cial activities, such as trade and tourism (23), arecrucial codeterminants of the probability that aspecies will be introduced and of the species’fate subsequent to the introduction to a newarea.

Stages of Invasions: Which SpeciesShould Management AddressSome background on terminology is essentialbefore we address issues relating to options for

managing biological invasions (see the sidebarDefinitions of Key Concepts and Terms inInvasion Ecology, with Special Reference toManagement Issues for definitions). We dealonly with those alien species that are successfulinvaders in the new regions (sensu References 8and 24). Many native species spread in responseto human actions, sometimes resulting in sub-stantially increased abundance and geograph-ical ranges. Such range expansions of nativespecies are important symptoms of environ-mental change, share some important featureswith spreading alien species, are considered un-desirable, and often require management inter-vention. Such range expansions of native speciesare, however, excluded from our discussion.Invasions of alien species form a special cate-gory of this environmental problem. It is usefulto conceptualize the status of alien species ina given region with reference to the above-mentioned naturalization-invasion continuum,a construct that invokes a series of barriers thata given species needs to negotiate in order tobecome alien, casual, naturalized, or invasive(Figure 2a). This scheme allows for the cat-egorization of the status of alien species usingonly objective biogeographical and ecologicalcriteria, rather than invoking human valuejudgments such as an assessment of impact(see, e.g., Reference 25). Many factors operateto allow alien species to overcome barriers, andthese factors must be considered when decidingon management options. Facilitation is one ofthese factors and is very important for deter-mining invasion success and its eventual extent(Figure 2b).

Adding a new species to an area oftenchanges the structure or functioning of thesystem. Such effects (generally termed impacts)may manifest at the level of populations orcommunities, whereas others, usually at laterstages of invasion, may produce ecosystem-level impacts (Figure 2c). Impacts of invasivespecies are sometimes rapid and dramatic,especially where they result in the transfor-mation of ecosystems. Examples are invasivegrasses that radically change fire regimes in


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many parts of the world, leading to ecosystemtransformation (26), and invasive insects thattransform ecosystem functioning by alteringcarbon, nutrient, and hydrologic cycles (27).When prioritizing species for control, effectson economic factors and ecosystem services arealso often considered. In many cases, adding aspecies to an ecosystem may seem to have nodiscernable effect, at least over short timescales.However, this may be misleading as effects areoften subtle but may have momentous conse-quences for ecosystem functioning over longertimescales, e.g., by disrupting plant reproduc-tive mutualisms with profound implications forfunctioning (28), or any of many effects of alienspecies that influence carbon sequestrationdynamics (29). Consequently, we separate con-siderations of invasiveness and invasion statusfrom those of impact. The latter often invokemany dimensions of human value systems(25).

Management must, however, consider allthe above factors. Key management optionsare prevention, early detection and eradication,containment, and various forms of mitigation.Mapping these onto the naturalization-invasioncontinuum defines several broad zones; these,and efforts toward preventing introductionsof potential invasive species, define the do-main of biosecurity (Figure 2d ). In most ar-eas, managers need to grapple with speciesat all stages of invasion, making prioritizationextremely complex. Finally, various forms ofanthropogenic change, synergisms, and non-linearities affect invasions in complex ways—invasional meltdown sensu Simberloff & VonHolle (30; see the box Definitions of KeyConcepts and Terms in Invasion Ecology,with Special Reference to Management Is-sues) (Figure 2e). These factors, combinedwith rapid changes associated with climatechange, must be borne in mind when assess-ing management options. This article addressesall these issues and reviews recent develop-ments in assessing and managing biologicalinvasions.

DEFINITIONS OF KEY CONCEPTS ANDTERMS IN INVASION ECOLOGY, WITHSPECIAL REFERENCE TO MANAGEMENTISSUES

Alien species: Those whose presence in a region is attributableto human actions that enabled them to overcome fundamen-tal biogeographical barriers (synonyms: exotic species, nonnativespecies). Some (a small proportion) of alien species form self-perpetuating populations in the new region. Of these, a subsetspread, or have the capacity to spread, over substantial distancesfrom introduction sites. Depending on their status within thenaturalization-invasion continuum, alien species may be termedcasual, naturalized, or invasive (8, 24).

Biosecurity: The management of risks posed by organisms tothe economy, environment, and human health through exclusion,mitigation, adaptation, control, and eradication.

Eradication: The extirpation of an entire population of a specieswithin a management unit. When a species can be declared erad-icated (how long after the management intervention) dependson the species and the situation and must take into account fac-tors such as seed-bank longevity (for plants). Eradication successshould be stated in terms of confidence limits that the species isnot present.

Impact: The description or quantification of how an alien speciesaffects both its environment and other organisms in the ecosys-tem. Parker et al. (31) proposed that impact should be conceptu-alized as the product of the range size of the invader, its averageabundance per unit area across that range, and the effect per in-dividual or per biomass unit of the invader.

Invasion ecology: The study of human-mediated introductionof organisms to areas outside the potential range of given organ-isms as defined by their natural dispersal mechanisms and biogeo-graphical barriers. The field deals with all aspects relating to theintroduction of organisms; their ability to establish, naturalize,and invade in the target region; their interactions with residentorganisms in their new location; and the consideration of costsand benefits of their presence and abundance with reference tohuman value systems (67).

Invasional meltdown: A term coined by Simberloff & Von Holle(30) to describe interactions among invaders that accelerate in-vasions and amplify their effects on native communities.

Invasive species: Alien species that sustain self-replacing pop-ulations over several life cycles; produce reproductive offspring,


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often in very large numbers at considerable distances from theparent and/or site of introduction; and have the potential tospread over long distances (8, 24).

Native species: Taxa that have evolved in a given area with-out human involvement or that have arrived there by naturalmeans, without intentional or unintentional intervention of hu-mans, from an area in which they are native (24).

Risk assessment: The determination of quantitative or quali-tative value of risk (the likelihood of an event occurring and theconsequences if it occurs). In the context of invasion ecology, riskassessment is undertaken to evaluate risks associated with a speciesbeing introduced (intentionally or accidentally) to a given re-gion, establishing itself, negotiating barriers in the naturalization-invasion continuum (Figure 2a), and having notable impacts.

IMPACT OF INVASIVE SPECIESAND ENVIRONMENTALCHANGE

Systematic studies of the impact of invasivespecies on invaded species, communities, andecosystems only started relatively recently, ashas the number of studies addressing practicalissues in this area and their proportional con-tribution to the invasion literature (Figure 3).Studies on impact have increased in importancefaster than those dealing with management asthe rapid escalation of problems first forcedinvasion ecology onto the agendas of conser-vation managers. Only recently has the scien-tific community realized that a better under-standing of the ecological impacts of invasivespecies is crucial for prioritizing managementefforts (31). Some recommended approachesthat could provide new insights include stud-ies that (a) measure impacts at multiple scalesand multiple levels of organization, (b) synthe-size available data on different response vari-ables, and (c) include models designed to guideempirical work and explore generalities (31).These approaches have stimulated considerableresearch over the past decade.

Information on impact is unevenly dis-tributed both in terms of geography andtaxonomy, corresponding to research biases ininvasion ecology in general (32). For mammals,invertebrates, and freshwater fish, research has

focused more clearly on impact than in othergroups. But a comparison of taxa by paperswith a focus on management issues, includingrisk-assessment, provides a different picture,showing that mammals, plants, and marineorganisms have received the most attention(Figure 4a). This pattern reflects differencesin the magnitude of ecological and economicimpacts among taxa (33) that are discussed indetail below. It also confirms the previous find-ing that, for invasive animals, impacts are morefrequently studied and cited than for plants (3).The geographical distribution of studies onimpact and management reflects the magnitudeof problems of biological invasions in partic-ular regions of the world and/or the level ofresources available for research, with Australia,New Zealand, and South Africa ranking highest(Figure 4b). These are the regions where mostresearch effort has focused on management,whereas research in Eurasian regions seems tofocus more on other questions or is still describ-ing basic patterns in understudied Asia (32).

Ecological Consequencesof Biological Invasions

The explosion of research on biological inva-sions has yielded global, continental, and/ornational reviews of ecological impacts for in-dividual taxonomic groups in both terrestrialand aquatic environments. Most studies havedealt with plants, and Levine et al. (34) haveprovided a synthesis of the mechanisms un-derlying the impacts from plant invasions.Some invasive plant species, transformers sensuRichardson et al. (8), affect the functioning ofecosystems by changing the availability of re-sources and the disturbance regimes of invadedecosystems. Specific topics that have been re-viewed include the impacts of hybridization ofnative and alien species (35), impacts of inva-sions on soil processes (36), impacts on na-tive species richness (37), and competition fromaliens with native plants (38). Other taxonomicand/or environmental groups for which the im-pact of alien species has been reviewed includefungi (39), insects (40, 41), earthworms (42),


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0

5

10

15

20

25

30

35

40

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1991-1995 1996-2000 2001-2005 2006-2009

Pro

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Figure 3Trends in studies on impact and management of invasive species indicate a gradual increase in research focustoward more practically oriented issues in the past 20 years. Values are percentages of the total number ofstudies that address impact and management, including risk assessment in five-year periods. Based on 8,004studies identified on the Web of Science by a search using the combination of terms alien, invasive, exotic, andnaturalized with taxonomic affiliations (see Figure 4a). (Note that the sum of the bars exceeds the combinedpercentages because some studies addressed more than one area of research.)

freshwater species (43), coastal marine biota(44), and mammals (45, 46). A review, focusedon the impact of invasions on interactions be-tween trophic groups, indicated that invasivespecies (via the introduction of alien pollina-tors, seed dispersers, herbivores, predators, orplants) frequently cause profound disruptionsto plant reproductive mutualisms (28). Thereis increasing evidence of severe impacts result-ing from invasive species infiltrating such net-works (e.g., Reference 47). Such impacts notonly have major implications for biodiversity,but also greatly complicate restoration effortsbecause the alien species frequently forge novelfunctions; when these disappear following con-trol efforts, unpredictable responses often occur(see below).

Despite a long-standing consensus that in-vasions pose a threat to native biodiversity, onlyrecently has the decline of native species at-tributable to biological invasions begun to beobjectively quantified. The impact of invasionon species diversity and the structure of invaded

ecosystems and communities has been mostlyanalyzed at a macroecological scale, usingregional or continental data. A meta-analysisof studies in Mediterranean-type ecosystemsworldwide revealed a significant negative ef-fect of invasions on native species richness (37).The strength of this effect depended on the lifeform of the invading plant, the invaded habitat,and the scale and character of the data. Studiesconducted at small scales or sampled over longperiods revealed stronger impacts than thoseat larger spatial scales and over shorter periods(37).

At the level of communities, only focusedstudies based on primary data can provide newinsights into the mechanisms of interactions be-tween invading species and recipient communi-ties. The decrease in species diversity of a plantcommunity owing to invasion was driven by theperformance of the invading species relative tothat of a native species dominating the com-munity before the invasion, rather than met-rics related to their ability to dominate the


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53.7

39.7 39.7

33.6

37.5 37.1

26.6

0

10

20

30

40

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60

Mammals(147)

Otherinvertebrates

(542)

Freshwaterfishes (237)

Marineorganisms

(128)

Plants (2,411) Insects (529) Birds (64)

Per

cent

age

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Impact

Management

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50.048.3

38.0 37.934.1 33.5 32.7

29.5 28.0

0

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60

Aus

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Sou

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community, such as height and cover. Becauseimpacts on species diversity at different scalesare correlated, a strong impact at the commu-nity level was associated with reduced speciesdiversity at higher scales; locally abundant in-vaders are also likely to be widespread at thelandscape scale (48).

The impact of biological invasions onspecies richness and diversity translates, via sev-eral processes, to biotic homogenization, whichreduces the distinctiveness of biological com-munities (49, 50), but this effect is scale de-pendent (51, 52). Over the past few centuries,globalization resulting from human activitieshas altered the composition of biotas throughtwo fundamental processes: extinctions and in-troductions. Global species extinctions lead toa continuous decrease of overall species rich-ness, i.e., γ-diversity (51). At the scale of conti-nents, regions, and countries, invasions exceedlocal extinctions and result in an increase inlocal or regional species richness (α-diversity)(53, 54). But as pointed out by Parker et al.(31), in the applied realm we make a distinc-tion between the species we care more aboutand those we like less. Winter et al. (52), inconsidering native losses and alien additions inconcert, showed that plant invasions in Euro-pean regions exceeded extinctions over the lastfew centuries, resulting in increased taxonomic,but decreased phylogenetic, diversity withinEuropean regions, and in increased taxonomicand phylogenetic similarity among Europeanregions. This is because extinct species werephylogenetically and taxonomically unique andtypical of individual regions, unlike the aliens.Consequently, European floras are losingtheir uniqueness. This shows that biodiversityneeds to be assessed, not only using standardtaxonomic metrics, but also by examining the

phylogenetic identity of species; the latter hasrarely been used as a metric of biodiversitychange over time (52).

Recent technological advances have facili-tated the assessment of impacts of invasions onthe structure of vegetation at large spatial scales.Asner et al. (55), using an airborne remote sens-ing system [high-fidelity imaging spectrome-ters (HiFIS) with light detection and ranging(LiDAR) sensors], mapped the location and im-pacts of five invasive plant species of differentfunctional types over more than 200,000 haof Hawaiian ecosystems. They showed thatthese species transform the three-dimensionalstructure of native rain forests, replacing na-tive species at different canopy levels. This workdemonstrates how the spread of invasive plantspecies can be monitored by remote sensingmethods, making it possible to determine eco-logical consequences of invasions and providingdetailed geographic information to guide con-servation and management efforts.

Ecosystem Servicesand Human Health

Biological invasions have many dramatic im-pacts, but also generate many subtle socio-economic consequences that are difficult to as-sess using traditional monetary approaches andmarket-based models (56). The MillenniumEcosystem Assessment (2) framework providesan opportunity to link ecological and economicimpacts by assuming that ecological changesimpact ecosystem services, hence human well-being. The ecosystem services approach at-tributes values to ecosystem processes as thebasis for human needs and distinguishes fourcategories: supporting (i.e., major ecosystem re-sources and energy cycles), provisioning (i.e.,

←−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−Figure 4Taxonomic and geographical differences in research focus of studies on biological invasions. (a) Percentage of studies, of the totalnumber published until 2006 (shown in parentheses), that addressed the impact of invasive species and their management, includingrisk assessment, is shown for particular taxonomic groups and (b) regions of the world. Ranking is based on the total contribution of allstudies that addressed impact, risk assessment and/or management shown above the bars, with values shown as percentages. (Note thatthe sum of bars exceeds the percentages above the bars because some studies addressed more than one area of research.) Based on a Webof Science search using the terms defined in Figure 3.


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production of goods), regulating (i.e., mainte-nance of ecosystem processes), and cultural (i.e.,nonmaterial benefits). The ecosystem assess-ment approach requires multidisciplinary col-laboration in environmental management (57).Alien species affect a wide range of ecosystemservices that underpin human well-being, in-cluding provisioning of food and fiber; regulat-ing the spread of human diseases; and provid-ing aesthetic, recreational, and tourism benefits(58, 59).

The disruption of ecosystem services as aresult of biological invasions is known to haveadverse socioeconomic, cultural, and humanhealth impacts. For example, a number of hu-man health problems, e.g., allergies and skindamage, are caused by invasive alien species(Table 1). Outbreaks of human diseases causedby novel pathogens, such as human immunod-eficiency virus (HIV), monkey pox, and severeacute respiratory syndrome (SARS), are anal-ogous to the process of biological invasions.These pathogens cross the barriers that sepa-rate their natural reservoirs from human popu-lations and ignite the epidemic spread of novelinfectious diseases (60), resulting in huge eco-nomic costs (61).

Looking at ecosystem services sheds light onthe overall magnitude and variety of impacts ofalien species and the implications for humanwell-being. Individual species and taxonomicgroups differ in the spatial extent of recordedimpact and in the variety of impact types. Thisis because impact is correlated with invasive-ness, which is generally associated with a widedistribution (32). Some European invaders,e.g., muskrat (Ondatra zibethicus), racoon dog(Nyctereutes procyonoides), thrips (Frankliniellaoccidentalis and Heliothrips hemorrhoidalis), orChinese mitten crab (Eriocheir sinensis), areknown to cause negative impact in as manyas 20–50 regions (33), while among plants, in-vaders with serious impact but localized distri-bution can also be found (62). The impact ofserious invaders is rarely restricted to a singleecosystem service; terrestrial vertebrates andfreshwater invaders exhibit the widest, but ter-restrial invertebrates the narrowest, range of

different types of impact (33). Van Wilgen et al.(63) presented the first national-scale assess-ment of impacts of invasive species on ecosys-tem services for invasive plants in five terrestrialbiomes of South Africa. They showed that, al-though measurable impacts on four out of fiveecosystem services are currently relatively low(only surface water runoff is strongly impactednow), impacts on all services (including ground-water recharge, livestock production, and bio-diversity) are increasing rapidly as invasions be-come more widespread.

Comparing Ecologicaland Economic Impacts

An alternative approach to case studies ad-dressing impact of individual species (Table 1)focuses on completeness and comparisonamong various groups of alien biota and isrepresented by geographically focused reviewssummarizing the impact of alien biota from anumber of taxonomic groups. Vila et al. (33)undertook such an exercise, drawing on therecently collated inventory of alien speciesfor Europe (64). This review looked at bothecological and economic impacts of invasionsand compared the quality of informationfor these two types of impacts for manytaxonomic groups. This study showed that,among terrestrial vertebrates and freshwaterplant and animal species, about 30% areknown to have ecological impacts that may beattributed to the preponderance of predatoryor omnivorous taxa among these two groups.Indeed, vertebrate predators on islands are theonly group of alien organisms whose invasionscaused the extinction of native species (notablybirds), and predation is a far more importantdriver of extinctions than competition (6, 65).Invasions in freshwater ecosystems often causetrophic cascades, and introduced predatorsseem to have greater effects owing to poordefense mechanisms and greater naıvete ofnative species toward novel predators (66).In contrast, only about 5.6% and 5.4% of allalien plants are documented to exert ecologicaland economic impact, respectively. However,


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because plants are the most numerous of allgroups analyzed, these values correspond tomore than 300 species with recorded impacts.The 342 terrestrial invertebrates accountfor 13.8% of all alien invertebrates, and thecorresponding values for marine biota are 172species for 16.1%. Relatively more terrestrialvertebrates (38.5%) and invertebrates (24.2%)have greater economic than ecological impact,whereas the opposite is true for freshwaterflora and fauna (only 24.3% of species causeseconomic impact). Generally, it appears thatecological and economic impacts of alienspecies are usually studied separately, butthey are likely to be highly correlated withintaxonomic groups. Nevertheless, the strengthof this correlation differs markedly amongtaxonomic groups, but the most importantdeviation from the rule is for terrestrial inver-tebrates, where consistently more species areattributed economic than ecological impactbecause the economic impact of invertebratesis most readily recognized. For plants, the re-verse is true, with ecological effects being morefrequently documented than economic effects,even though the former are less tangible (33).

In general, more species are known to causeeconomic than ecological impacts because theformer are more easily perceived and are morelikely to be quickly reported by stakeholders,and economic pests are likely to attract morescientific attention (33). In fact, it is the impactof a species that largely determines whetheror not it is studied. Invasive species with thegreatest numbers of published case studies haveserious economic impact; zebra mussel (Dreis-sena polymorpha), Argentine ant (Linepithemahumile), and spotted knapweed (Centaurea mac-ulosa) are the most prominent examples. Suchresearch focus in turn leads to better under-standing of their ecological impacts (32).

The European overview (33) indicated thatimpact has been described and documented inthe literature for only about 10% of the to-tal number of aliens in Europe (up to 11,000taxa; see Reference 64). Although only a frac-tion of these are invasive owing to their lossesduring transitions between stages of the inva-

sion process (Figure 2b), the real number ofaliens exerting ecological impacts is probablyhigher, and impact remains to be documentedfor many invasive species because any success-ful invasive species that achieves dominance inan ecosystem is likely to have an ecological im-pact. Impact seems to be underestimated par-ticularly for species-rich taxa and across largeregions. One of the major constraints to stan-dardized measures of impact is that, even in thebest-studied regions such as Europe, we knowabout impact for only a very small proportion ofinvaders (33). The same applies for other well-studied regions like South Africa (67).

Impacts in Monetary Terms

The economics of biological invasions hasbecome a hot research topic in the past decade(e.g., References 61 and 68), and cost-benefitanalyses conducted for individual species haveprovided detailed insight into the costs imposedby some invasions (e.g., References 69 and 70).To translate ecological information into sum-mary monetary terms for regions or continents,it is necessary to know the number of alienspecies causing ecological and economic im-pacts. Although such information is currentlyavailable for Europe (33), until recently, thiscontinent lagged behind North America in be-ing able to directly quantify financial impacts.Several attempts have been made to quantifythe costs of biological invasions since the firstestimate of US$97 billion per year in damagesfrom 79 alien species for the period 1906–1991in the United States (71), including the updateto US$120 billion for the United States (72).Sinden et al. (73) estimated that weeds alonecost AUS$3.9 billion per year in lower farmincomes and higher food costs in Australiaand that costs to central and local governmenton monitoring, control, management, andresearch on weeds was at least AUS$116.4million each year. In South Africa, invasionshave been shown to reduce the value of fynbosecosystems (∼4% of the country) by overUS$11.75 billion (74).


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Tab

le1

Exa

mpl

esof

vari

ous

type

sof

impa

ctof

inva

sive

alie

nsp

ecie

son

hum

anhe

alth

(I–V

I)an

dso

cial

acti

viti

es(V

II–V

III)

cate

gori

zed

acco

rdin

gto

taxo

nom

icgr

oups

and

envi

ronm

ent

Typ

eof

impa

ctP

lant

sSa

ltw

ater

inve

rteb

rate

sFr

eshw

ater

anim

als

Ter

rest

rial

inve

rteb

rate

sV

erte

brat

esI.

Cau

seor

vect

orof

hum

andi

seas

esor

ailm

ent

Aila

nthu

salti

ssim

aa(lo

ngex

posu

reto

sap

can

caus

em

yoca

rditi

s),R

obin

iaps

eudo

acac

ia(t

oxin

sin

flow

ers

and

seed

prov

oke

gast

roen

teri

tis)

Ale

xand

rium

cate

nella

a

(poi

soni

ngfr

omco

nsum

edsh

ellfi

shca

nle

adto

deat

h),

Stye

lacla

vaa

(res

pira

tory

prob

lem

sfr

omsp

rays

dam

age

tissu

es)

Eri

oche

irsin

ensis

a(in

nativ

era

nge

aho

stfo

rth

elu

ngflu

kepa

rasi

te,c

ausi

ngdi

seas

esof

lung

san

dot

her

body

part

s),

Proc

amba

rusc

lark

iia

(hos

tfor

trem

atod

esth

atar

epo

tent

ial

para

site

sof

hum

ans)

Aed

esal

bopi

ctus

a

(arb

ovir

uses

,pl

asm

odia

,fila

rias

is)

Nyc

tere

utes

proc

yono

ides

a

(rab

ies,

tric

hine

llosi

s),

Ond

atra

zibe

thicu

sa

(lept

ospi

rosi

s,ce

stod

e),

Proc

yon

loto

ra(r

acoo

nro

undw

orm

),R

attu

sno

rveg

icusa

(lept

ospi

rosi

s,he

patit

is),

Sciu

rus

caro

linen

sisa

(squ

irre

lpo

xvir

us),

Tam

iass

ibir

icusa

(pot

entia

lvec

tor

for

Lym

edi

seas

e),T

rach

emys

scrip

taa

(sal

mon

elos

is)

II.H

osto

fpar

asite

sof

pets

and

lives

tock

——

—A

rion

vulg

arisa

(nem

atod

es)

Cer

vusn

ippo

na(n

emat

odes

,bo

vine

tube

rcul

osis

),N

ycte

reut

espr

ocyo

noid

esa

(rab

bies

,sar

copt

icm

ange

)II

I.C

ause

sin

juri

esC

orta

deri

ase

lloan

a,a

Spar

tina

angl

ica(c

uts

byle

aves

),C

aesa

lpin

iade

cape

tala

,Ros

aru

gosa

aan

dm

any

othe

rsp

ecie

s(t

horn

yth

icke

ts)

Bala

nusi

mpr

ovisu

s,a

Ens

isam

erica

nusa

(sha

rpsh

ells

infli

ctcu

ts),

Siga

nus

rivu

latu

s,aR

hopi

lem

ano

mad

icaa

(pai

nful

stin

gs)

Dre

issen

apo

lym

orph

aa

(sha

rpsh

ells

infli

ctcu

ts),

Plot

osus

linea

tus

(inju

ries

caus

edby

the

barb

edan

dve

nom

ous

dors

alsp

ine)

—Bo

iga

irre

gula

ris(

snak

ebi

tes)

IV.C

ause

sal

lerg

ies

Aca

ciade

alba

ta,a

Cor

tade

ria

sello

anaa

(pol

len

alle

rgy)

,A

ilant

husa

ltissi

maa

(der

mat

itis)

,Am

bros

iaar

tem

isiifo

liaa

(pol

len

alle

rgy,

derm

atiti

s),

Her

acle

umm

ante

gazz

ianu

ma

(der

mat

itis)

,Sch

inus

tere

bint

hifo

lius(

flu-l

ike

sym

ptom

s,sn

eezi

ng,s

inus

cong

estio

n)

—C

erco

pagi

spen

goia

(may

caus

eal

lerg

icre

actio

nsin

fishe

rman

whe

nth

eycl

ean

thei

rne

ts)

Lym

antr

iadi

spar

(hai

rson

larv

aean

deg

gm

asse

sca

use

alle

rgie

s),S

olen

opsis

invi

cta

(stin

gsar

epr

one

toin

fect

ion

and

som

etim

esca

use

anap

hyla

ctic

reac

tions

)

—


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V.A

ccum

ulat

ion

ofto

xins

and

thei

rtr

ansf

erto

hum

anfo

od

Rho

dode

ndro

npo

nticu

ma

(poi

sono

usho

ney

can

caus

eca

rdia

cpr

oble

ms)

,Ech

ium

plan

tagi

neum

(hig

hco

ncen

trat

ions

ofpy

rrol

izid

ine

caus

esho

ney

mad

eex

clus

ivel

yfr

omth

issp

ecie

sto

beto

xic)

—N

eogo

bius

mel

anos

tom

us,a

Proc

amba

rusc

lark

iia

(hea

vym

etal

san

dcy

anot

oxin

s)

——

VI.

Haz

ard

tohe

alth

byco

ntam

inat

ion

ofso

ilan

dw

ater

——

——

Bran

taca

nade

nsisa

(exc

essi

vedr

oppi

ngs)

VII

.Im

pede

sre

crea

tiona

lac

tiviti

esan

dto

uris

m

Spar

tina

angl

ica,H

erac

leum

man

tega

zzia

num

,Ros

aru

gosa

(for

min

gim

pene

trab

lest

ands

),E

ichor

nia

cras

sipes

and

man

yot

her

aqua

ticw

eeds

(cov

erw

ater

bodi

es,i

mpe

ding

recr

eatio

nan

dtr

ansp

ort)

Ale

xand

rium

cate

nella

a

(cau

sing

red

tides

)—

Line

pith

ema

hum

ile,

Sole

nops

isin

vict

a(it

chy

stin

gs),

Ves

pula

germ

anica

,V.v

ulga

ris

(att

ack

and

stin

ghu

man

sw

hen

defe

ndin

gth

eir

nest

s,m

akin

gou

tdoo

rre

crea

tion

unpl

easa

ntan

dha

zard

ous)

—

VII

I.A

esth

etic

impa

ct,

dete

rior

atio

nof

the

qual

ityof

envi

ronm

ent

Seir

idiu

mca

rdin

ale

(tre

e-ki

lling

fung

us),

Cod

ium

frag

ilesu

bsp.

tom

ento

soid

esa

(rot

ting

bran

ches

onbe

ache

sca

use

offe

nsiv

ese

ptic

-sm

ellin

gm

etha

nega

s)

——

Ano

plop

hora

chin

ensis

,A

.gla

brip

enni

s,C

amer

aria

ohri

della

(kill

ing

tree

s),

Har

mon

iaax

yrid

is(s

war

ms

onbu

ildin

gs)

Ele

uthe

roda

ctyl

usco

qui(

nois

edi

stur

banc

e),O

ndat

razi

beth

icusa

(dam

age

tori

verb

anks

),Ps

ittac

ula

kram

eria

(noi

sedi

stur

banc

e)

a Bas

edon

data

from

the

DA

ISIE

port

al(h

ttp:

//w

ww

.eur

ope-

alie

ns.o

rg).


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In Europe, cost-benefit analyses are scarce.Most have focused on individual species orsectors, whereas for some harmful invaderswidespread across the whole of Europe, no costanalyses have been made. Most expenses gen-erated by invaders are in the form of man-agement costs, including eradication, control,monitoring, and environmental education pro-grams (see Reference 33). For South Africa,species-specific costs of management are avail-able for the national Working for Water pro-gram. These show that 57% of funds (out ofa total of US$48 million for 2002–2003) werespent on clearing invasive trees (targeted be-cause of their impact on surface water runoff),with large sums also spent on clearing speciessuch as Chromolaena odorata, Lantana camara,and Opuntia spp., which are targeted for theirimpacts on biodiversity and other ecosystemservices (75). For Europe, the total costs ofinvasive alien species are estimated to be atleast €12.5 billion per year and probably over€20 billion per year if extrapolated, and this islikely to be a significant underestimate of thereal situation. The most affected sectors includeagriculture, fisheries and aquaculture, forestry,health sectors, and nature conservation; inva-sions of some species also caused declines inrecreational or cultural heritage values associ-ated with various landscapes and water bod-ies (59). Although financial costs are difficultto compare across regions owing to the lack ofdata for many significant invaders and unevendistribution of information among different ge-ographic areas (33), the recent assessment ofeconomic costs provides a basis for the devel-opment of an EU Strategy on Invasive AlienSpecies (59).

Of course, alien species also offer economicreturns in some sectors, for example, fast-growing alien trees for commercial forestry orby satisfying the demand for exotic products,pets, and garden plants. However, a growingbody of evidence suggests that in many casesthe invasion-related costs, even for species ofmajor commercial importance [e.g., in the caseof Acacia mearnsii in South Africa (76)], mayoutweigh the benefits. The pioneering study

of Pimentel (61) showed that costs incurredby biological invasions globally amounted toabout 5% of the global gross domestic product(GDP).

Limitations of Measuring Impact

Until the late 1990s, little formal attention wasgiven to defining impact or connecting ecolog-ical theory with particular measures of impact.The paper by Parker et al. (31), stimulated bythe need for a general framework for under-standing and predicting impacts of invasions,suggests that the total impact of an invaderincludes three fundamental components:(a) range, (b) abundance, and (c) the per capitaor unit of biomass effect of the invader. Becauseboth the population dynamics of an invaderand that of native species vary over space andtime, as well as with respect to environmentalsettings, the estimate of an invader’s impact islikely to depend on the spatial and temporalscale of a study as envisaged by the boom-and-bust dynamics of some invaders (31, 37, 51).This makes impact of individual invaders veryvariable and dependent upon (a) the identity ofinvading species; (b) the structure, composition,and functioning of the invaded communities;(c) the environmental settings, such as climate,soil, or water quality; and (d ) the interaction ofthe three over space and time.

This context dependency makes measuringimpact particularly difficult and complex, moreso than objectively defining measures for nat-uralization or invasiveness (8, 24). Comparedto our much-improved understanding of theprinciples and mechanisms of biological inva-sions (e.g., Reference 5), impact remains ratherpoorly conceptualized and documented. Thelament for the lack of a general, universally ap-plicable framework expressed by Parker et al.(31) still applies.

There are additional issues that hinderprogress toward standardized measures of im-pacts. One is that impacts of invasive speciesare often labeled negative or positive, introduc-ing difficulties associated with value judgments.For effects of invasive plants on native plants


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and animals, this is relatively straightforward;reduced values in population and communitycharacteristics imply decreased vigor and pop-ulation status of affected native biota. How-ever, elevated levels of certain soil nutrients,for example, may not necessarily mean an im-proved state of the affected ecosystem. On theone hand, in oligotrophic ecosystems, increasednutrient status may lead to further invasion (77).On the other hand, elevated nutrient levels canresult in increased structural complexity of veg-etation, especially if coupled with introductionof a new life form, thereby providing habitatfor new species or local species suffering fromdestruction of their native habitats (78). Inva-sive plant species cause many types of changesto fire regimes by altering the type and spa-tial arrangement of fuels. Changes may resultin increased or decreased fire frequencies andchanges in the type of fire (surface versus crownfires), with many potential implications for theecosystem that cannot be classified as negativeor positive (26). Generally, invasive species thatadd a new functional type to an ecosystem havea greater impact (and are often responsible forrapid ecosystem-level changes) than those thatdiffer from natives only in traits, such as lit-ter quality or growth rates, that are distributedcontinuously among species. Many profoundimpacts attributable to invasive species occurwhen introduced species act as hubs in com-munity networks or keystone species.

Complex impacts of invasive species canresult from effects that ripple and reboundthrough trophic levels. For example, many inva-sive plants change vegetation structure, therebyproviding altered habitat for other species.There are many records of vertebrates, particu-larly birds and mammals, responding in variousways to invasion-induced changes to vegetationstructure. For instance, the American Robin(Turdus migratorius) when nesting in two inva-sive plant species (Lonicera maackii and Rhamnuscathartica) experienced higher predation thanin nests built in comparable native shrubs andtrees. Schmidt & Whelan (78) attributed this tolower nesting height in the invaded areas, theabsence of sharp thorns on the alien species,

and possibly branch architecture that facilitatedpredator movement among the alien species.Invasion-induced changes to habitat may trans-late to important functional changes in ecosys-tems. For example, in arid savannas in SouthAfrica, replacement of native Acacia species byinvasive alien Prosopis species changes habi-tat structure, notably the canopy architectureand availability of perches for frugivorous birds(79), thus altering the prevailing bird-mediatedshrub nucleation processes in these ecosystems(47). Grosholz & Ruiz (80) review the currentunderstanding of multitrophic effects of inva-sions in marine and estuarine systems. Althoughthe evidence for impacts across trophic levelsin estuarine and marine systems is still limitedcompared to terrestrial systems, the effects ofmarine invasions may commonly cross trophiclevels. The magnitude of the effects vary, andimpacts need to be viewed as having multipleattributes that reside along a continuum ratherthan existing as residing in binary states of “im-pact” or “no impact” (80).

It appears that simple scoring systems, whichare based on the number of impact types (33),provide the most robust results and capturelarge-scale patterns and differences among tax-onomic groups. In another study, Nentwiget al. (81) applied a generic scoring system tocompare impacts of alien mammal species inEurope, with the aim of identifying the mostharmful species to aid in prioritizing conserva-tion measures to ameliorate their negative ef-fects. They classified impact as environmentalor economic, and within each category, theydistinguished five types of impact: ecologicalimpact (which is through competition, preda-tion, hybridization, transmission of disease, andherbivory) and economic impact (which is onagriculture, livestock, forestry, human health,and infrastructure). Each species was scoredfor each impact type on a five-degree scale,and ranking was performed by summing up thescores across categories of impact types. By in-cluding information on actual distribution, itwas possible to assess individual invasive mam-mals and relate their impact to species traits.Of these traits, ecological flexibility (measured


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as the number of different habitats a species oc-cupies) was the best predictor of impact (81).The scoring system was robust in terms of theoverall result in spite of having insufficient in-formation available for some categories of im-pact; thus this scoring can be adjusted for thepurpose of different stakeholder groups and canbe adapted to other taxonomic groups. A sim-ilar system of impact assessment has been de-veloped for marine biota in the Baltic Sea (82).

MANAGEMENT OFBIOLOGICAL INVASIONS

The harmful effects of invasive alien species arenow widely recognized, and multiscale (local,regional, national, and international) programsare in place in many parts of the world toreduce current and potential future impacts.For example, the European Union has sup-ported 49 major projects that address differentaspects of biological invasions since 2000 (83),including three pan-European projects. Thesewere aimed at collating available informa-tion at the continental scale (64), analyzingthe role of biological invasions as a driverthreatening biodiversity (the ALARM project),and improving risk-assessment schemes (84).Many countries have launched far-reachingintegrated strategies for dealing with biologicalinvasions that include initiatives for preventingthe arrival of new alien species with a high riskof becoming invasive (or at least reducing therate of introductions of such species); detectingand responding rapidly to new invasions,containing invasions where eradication is notfeasible; reducing extent and impacts of thoseinvasive species that are already widespread;and restoration of areas degraded by invasivespecies. National initiatives take very differentforms in different countries. National strate-gies are advocated, e.g., in the Global InvasiveSpecies Program’s Global Strategy (1), andsome are in place. For example, Australiahas an Australian Pest Animal Strategy andan Australian Weeds Strategy, the Bahamashas a National Invasive Species Strategy,New Zealand has a Biosecurity Strategy, and

the United States has a National Strategyand Implementation Plan for Invasive SpeciesManagement and the National Invasive SpeciesCouncil’s Action Plan for the Nation. At thesupranational level, the European Union hasrecently confirmed its commitment to worktoward having a European strategy on inva-sive alien species, including a pan-Europeaninformation system for invasive alien species,in place in 2010 (85). Such strategies arerecent developments, and many dimensionsof biosecurity are poorly understood and thesubject of much research effort (86).

There has been a proliferation of approachesaimed at assisting managers in assigning prior-ity to species and areas as well as at improvingthe efficiency of management interventions.There is a massive literature on these topics.We review some approaches and developmentsin this sphere, with special emphasis on fouroverlapping areas that we consider to beparticularly important: risk assessment (mainlypreborder, but increasingly with postincursionapplications), pathway management, early de-tection and rapid response, and mitigation andrestoration.

Risk Assessment

Risk assessment is the first step in the riskmanagement process. Formal risk assessmentprocedures were initially developed in areassuch as public health, banking, engineering,and pollution control, but much work has beendone recently on developing risk assessmentframeworks for biosecurity (84, 86). Preventingthe introduction of species with a high risk ofbecoming invasive is, in theory, the most cost-effective management strategy (Figure 2d ).Border interception data for terrestrial insectsin Europe suggest that many more agricul-tural and domestic pests are intercepted thanspecies associated with natural habitats (87);the preborder risk assessment therefore hasthe potential to intercept alien insects withpotentially high economic impact. Key con-siderations in risk assessment development forbiosecurity have been the inherent difficulty of


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predicting species invasiveness in a changingworld, the limited availability of data known tobe important for determining invasiveness, andaccommodating sociopolitical issues in riskassessment frameworks. Because many alienspecies are intentionally introduced for theircommercial or other value to humans, highlyconservative risk assessments are often op-posed by those who stand to benefit from suchspecies. Global trade agreements generallypreclude exclusion of species on the basis ofthe precautionary principle, and there hasbeen a strong focus on developing objective,science-based criteria for risk assessments,drawing on advances in invasion ecology andrelated fields. Most attention has been focusedon organism-based protocols, and screeningprocedures with good accuracy rates (>80%in many cases) are now available for diverseregions and taxa (Figure 4), e.g., fish in theLaurentian Great Lakes (88), fish in California(89), plants in many parts of the world (90),and birds in New Zealand (91). As a result, theproportion of papers addressing risk assessmenthas been steadily increasing in the invasionliterature since the early 1990s (Figure 3).

One reason for the improved accuracyof such screening systems is the increasedavailability of databases of introduced speciescovering large regions with objective catego-rization of the invasive status of species (64, 92).The Australian border weed risk assessmentsystem, implemented by Pheloung et al. (93)in 1997 to reduce the high economic costs andmassive environmental damage associated withintroducing serious weeds, was tested, some-times with slight modifications (94), in otherregions of the world: Hawaii and the PacificIslands, central Europe, Japan, and Florida. Acomparison of the results of these trials revealedsimilar levels of accuracy (90), but differences ininterpretation of the questions reduce the con-sistency of application. A modification of thequestions was therefore suggested to make thesystem universally applicable (95). Such effortsare important because preborder screeningsystems are improved through usage. Weberet al. (96) reviewed the behavior of the weed

risk assessment system with reference to datacollected from the assessment of species pro-posed for importation or held within geneticresource centers in Australia over eight years.They found that of the 35 variables assessedby the questions, 5 gave the same outcome asthe full model for 71% species: unintentionalhuman dispersal; congeneric weed; weed else-where; tolerates or benefits from mutilation,cultivation, or fire; and reproduction by vegeta-tive propagation. Although information on thehistory and behavior of introduced species inother regions is a crucial component of effectivescreening, and better global data translate intobetter predictions, the weed elsewhere variablewas not the first splitting variable in this model,indicating that the weed risk assessment systemcan identify high-risk species with no history ofweediness (96).

Improved risk assessment frameworks areresulting in wider acceptance of preborderscreening protocols and their formal incorpo-ration in many legal instruments and policies.In a landmark study, Keller et al. (97) showedthat the use of the weed risk assessment sys-tem in Australia provides net economic bene-fits by allowing authorities to screen out costlyinvasive species. Even after accounting for lostrevenue from the small percentage of valuablenonweeds that may be incorrectly rejected, theyshowed that screening could save the countryUS$1.67 billion over 50 years.

Until recently, formal risk assessment pro-cedures for invasive species were mainly ap-plied only to preborder assessments. In the lastdecade or so, they are also being applied at laterstages of the naturalization-invasion continuum(Figure 2d ). Examples of the many interest-ing and important research areas in this direc-tion are the evaluation of critical uncertaintythresholds for spatial models of invasion risk(98), special approaches for dealing with uncer-tainty in data-poor systems (99), and the incor-poration of insights from molecular techniques(100). Much progress has been made towarddeveloping risk maps that apply a range of ap-proaches for modeling invasive spread in frag-mented landscapes and predicting areas that are


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at a high risk of invasion or could be in thefuture. These efforts draw on advances in re-mote sensing (e.g., Reference 101), modelingmethods, and computing. Some examples arethe spatially explicit modeling of invasion riskfor commercially important alien trees at a na-tional scale (102); assessing the risk of invasiveplants spreading along riparian zones into pro-tected areas (103); a risk map for invasions ofalien mussels (Dreissena spp.) in the contiguousUnited States on the basis of calcium concen-tration data from over 3,000 stream and riversites (104); and modeling the risk of the emer-ald ash borer (Agrilus planipennis) spreading inOhio, combining the insect’s inherent dispersalcapabilities with options for human-facilitatedlong-distance dispersal (105).

An invasion-risk map for Europe, which isbased on levels of plant invasion in 33 habitattypes (106), projects future invasions under arange of socioeconomic scenarios. It appearsthat the implementation of environment-friendly oriented policies has little scope forautomatically restricting the spread of alienplants. This suggests that effective managementof invasions require specific policy approachesover and above the generic ones that are cur-rently on the policy agenda (107). A Web-basedtool was recently developed for the Baltic Sea,based on a “biopollution index” that classifiesimpact of invasive alien species on nativespecies, communities, habitats, and ecosystemfunctioning. The assessment can be used toevaluate management performance whereavoidance measures were necessary and canassist in preventing further unwanted introduc-tions. Moreover, the simple scoring system pro-vides opportunities for repeated assessment ofthe same region and thus can be used to monitorthe efficiency of management measures (82).

Much work has focused on risk identifi-cation and assessment for specific taxa, e.g.,plants (90, 108), freshwater invertebrates (109),mussels (110), fish (111), reptiles, and amphib-ians (112–114). Each taxon has its own set ofcharacteristics that defines and limits optionsfor risk assessment. These include the size ofthe organisms, their detectability and degree of

taxonomic resolution, their links with specifictransport vectors, their usefulness to humans,and their potential to cause undesirable impacts(the greater the potential impact, the greater themotivation for robust risk assessment). Anotherstrong research focus has been on risk identi-fication and assessment for specific sectors andvectors, such as biofuels (e.g., Reference 115),and shipping-related agents, such as ballast wa-ter (116) and hull fouling (117). The combina-tion of environmental niche- and vector-basedmodels seems to offer more precise estimates ofinvasion risk than can either of these approachesalone, as illustrated by the Chinese mitten crab(Eriocheir sinensis) (118) and a study of SouthAfrican native plants invading other parts of theworld, which combined niche-based modelingand proxies of propagule pressure derived fromtrade volumes and tourism (23). Much work isunder way on integrating taxon- and sector- orvector-based assessment protocols, and insightsfrom such work will probably have substantialinfluence in shaping policies.

Pathway and Vector Management

In many instances, the best or only way ofreducing introductions is to manage vectorsand pathways. This is a relatively recentfocus (119) and the subject of much ongoingresearch. Pathway and vector management isrequired to reduce colonization pressure, sensuLockwood et al. (120), in several ways. First,once pathways and vectors of introduction anddissemination are identified, various proactivemeasures can be implemented. For instance,the commercial trade in ornamental plants isa major (often the primary) pathway for theintroduction and dissemination of invasivealien plants; the most serious plant invadersresult from garden escapes (62, 121, 122).Elucidation of the dimensions of this pathwaypave the way for a suite of interventions,ranging from increasing public awareness ofproblems, finding alternatives for invasivespecies (123), and applying biological control,to improving measures of detection andpolicy enforcement. Similarly, shipping is the


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primary pathway for introductions of aquaticorganisms, mainly invertebrates (9, 124), andelucidation of the vectors that are implicatedallows for targeted management. However,propagule pressure associated with particularpathways is difficult to quantify, and solid dataare only starting to appear. Lee & Chown (125)report that over 1,400 seeds from 99 taxa aretransported to Antarctica each field season withpassenger luggage and cargo and that 30% to50% of these propagules enter the recipient en-vironment. Good knowledge of pathways andvectors also opens other options for limiting thecontamination of vectors (e.g., through controlof pest populations in source regions), pathwaymonitoring for target pests, and genericmanagement measures that may have addedbenefits beyond the target pest species (e.g.,hull cleaning and antifouling, ballast waterexchange). Such interventions have the poten-tial to reduce propagule pressure and thus thelikelihood of establishment and spread. Eluci-dation of introduction pathways is also crucialfor informing various facets of postincursionmanagement, for example, by predicting thegenetic diversity of the alien species, which hasimplications for their spread and control (126).

An important issue relates to responsibili-ties for invasions resulting from particular path-ways. Hulme et al. (9) suggest the followingallocation of responsibilities among applicants,exporters, importers, carriers, and developersregarding different pathways of introduction:

� Release (alien organisms introduced asa commodity and deliberately released,e.g., biocontrol agents, game animals,plants for erosion control) is the respon-sibility of the applicant;

� Escape (alien organisms introduced as acommodity but escaping unintentionally,e.g., feral crops and livestock, pets, gardenplants, live baits) is the responsibility ofthe importer;

� Contaminant pathway (unintentional in-troduction with a specific commodity,e.g., parasites and pests of traded plantsand animals) is the responsibility of theexporter;

� Stowaway (unintentional introductionwith transport vector) is the responsibilityof the carrier;

� Dispersal corridors (artificial corridorsamong marine basins) is the responsibilityof the developer; and

� Unaided pathway (unintentional intro-duction through natural dispersal ofaliens through political borders) is the re-sponsibility of the polluter.

The first two pathways are subject to na-tional regulations, whereas the others requireinternational policies (9). This is one area whereeffective biological management demands com-plex multisector and multinational collabora-tion, and much work remains to be done in thisarea. Success in such ventures holds the key toreducing the influx of alien species.

Early Detection and Rapid Response

The multiple pathways of introduction andthe huge volume of traded commodities makethe interception of all potentially invasive alienspecies unrealistic. Early detection and rapid re-sponse initiatives are therefore a crucial ingre-dient of integrated programs for dealing withinvasive species.

Rapid response must be triggered by earlydetection (83). An obvious problem is thatemerging invaders are rare; in many cases,such low occurrence fundamentally com-promises detection. The problem is greaterwhen the organisms are small, inconspicuous,or otherwise difficult to see, identify, andmap. Much has been done in this area onnumerous fronts. Research has focused onimproving protocols and technologies forremote sensing and on developing their use formonitoring alien species (127) and mapping(128). Increasingly robust protocols are beingdesigned for surveys, e.g., to quantify theprobability that a given surveying techniquewill detect a target species if it is present(129). Advanced modeling has been appliedto identify key sites of incursions or highabundance, e.g., to focus early detection effortsusing networks of volunteers to locate invasive


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plants in the northeastern United States (130).For small aquatic organisms, detection can beoptimized using risk-based sampling designscombined with high-sampling intensity inareas deemed most vulnerable to invasion,rather than less intensive sampling at moresites (131). Because it is often less effective torespond to rare incursions than to those abovesome abundance threshold, defining areas ofpotential dominance is useful (132). Better,more user-friendly identification guides areimportant tools, e.g., for plants and seeds (133).Many new high-tech diagnostic tools have beendeveloped for detecting even small numbers ofmicroorganisms. These include gene probes(e.g., for plankton trawls) (129), DNA barcod-ing (134), and acoustic sensors (e.g., to detectAsian long-horned beetles) (135). An exampleof an attempt to integrate various availabletools to assist in detection is the Cactus MothDetection and Monitoring Network, whichmonitors incursions of Cactoblastis cactorum inthe southern United States and Mexico (http://www.gri.msstate.edu/research/cmdmn/).Several invasive species atlas projects haveearly detection initiatives, e.g., the InvasivePlant Atlas of New England (136).

The issue of early detection highlights thecrucial role of taxonomy in invasion biology. Inmany regions, alien species come from all overthe world. Identifying these species is a majorchallenge, and misidentification can have seri-ous consequences. No rigorous studies are pos-sible in any field of biodiversity/biogeographyin the absence of good taxonomy, and this isequally true for biological invasions. Capacitybuilding for taxonomy of alien organisms is ur-gently needed (137).

Eradication

Biological control has become and will remainthe foundation of sustainable control effortsfor many invasive species, especially plants, inmany regions. However, there is renewed in-terest in eradication, following a period whenthe prevailing view was that eradication wasvery seldom achievable. Simberloff (138) has

argued that pessimism about the prospects oferadicating invasive species was fostered by thewidespread publicity of failures, but he believesthat eradication should be attempted more of-ten. Mammals are relatively easy to eradicate,and many successful eradications have beenreported, mainly from islands for cats, foxes,goats, rats, and other mammal species (139).Several (apparently) successful eradications ofinvasive species from diverse taxonomic groupsaround the world have been reported recently(138). Among the most widely cited projectswere those on the seaweed Caulerpa taxifo-lia [eradicated from a lagoon in California in2006 (140)] and the marine mussel Mytilop-sis sallei [eradicated from a harbor in northernAustralia (138)]. There are relatively few re-ports of successful eradications of invasivealien plants. Simberloff (138) singles out agrass Cenchrus echinatus, eradicated from anHawaiian island, and a herb Bassia scoparia, fromAustralia, as noteworthy examples of recent suc-cessful plant eradications.

Rejmanek & Pitcairn (141) reviewed aunique data set on eradication attempts by theCalifornia Department of Food and Agricul-ture involving 18 plant species and 53 separateinfestations targeted for eradication in theperiod from 1972 to 2000. They show that thelikelihood of eradication declines rapidly withan increasing area of infestation. Generalizingfrom these data, they suggest that professionaleradication of infestations smaller than onehectare is usually possible. For infestationsof 1–100 ha, the success rate was about 30%,whereas for infestations 101–1,000 ha in size,25% of the efforts were successful. Costsof eradication projects increase dramaticallyas the size of the infestation increases. TheCalifornian data suggest that eradication ofspecies occupying >1,000 ha is very unlikely,given the resources typically committed tosuch operations. Many eradication efforts failbecause of poor planning and execution. Thepicture to emerge from a review of the outcomeof plant eradication efforts on the GalapagosIslands (142) is relevant worldwide. Of 30 erad-ication projects covering 23 potentially invasive


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plant species with limited distributions on fourGalapagos islands, only 4 were successful. Fail-ures were attributed to inadequate attention toone or more of the following factors: adequatereview of international information on thebiology and management options for the targetspecies; obtaining permission from relevantlandowners and securing cooperation from thecommunity; mapping the total distribution ofthe target species at the start of the project; edu-cating stakeholders about biological invasions;planning resources for the full duration of theproject; regular project evaluation; and consid-ering eradication as one tool in a restorationtool box. Much research is currently underwayto provide support for eradication efforts (143).

Mitigation and Restoration

Much effort has been spent on developingstrategies and approaches for restoring ecosys-tems following degradation caused by invasivespecies. Interventions range from low-impactpractices, involving only the removal or reduc-tions in numbers of invasive species througha myriad of manipulative treatments aimed atreducing the presence, abundance, or impactsof invasive species and favoring native species,to massive and expensive exercises, involvingengineering, reintroduction of native species,and various attempt to direct succession. Manyrestoration efforts have succeeded in mitigatingnegative impacts of invasive species with impor-tant benefits (e.g., Reference 144).

An emerging problem relates to what hap-pens in, or to, ecosystems once invasive speciesare removed (145). This issue has many di-mensions. There are increasing reports of “sec-ondary invasions,” the rapid replacement of theremoved invasive species by others that capi-talize on the disturbance caused by the controloperations and/or resource alteration caused bythe invasive species or the management inter-vention (e.g., Reference 146). Related to thisis the problem of “legacy effects,” long-lastingchanges to the ecosystem that persist after theremoval of the invasive species, e.g., elevatednitrogen (N) levels in the soil following inva-

sions by N-fixing plants (77, 147) or changedmicrobial conditions (148). Such legacy effectsare important contributors to “invasional melt-down” (30) and seem set to cause increasingproblems for restoration following invasion.

Restoration involving the removal of in-vasive species changes the character of habi-tats (145). There are many records of na-tive species being disadvantaged by invasivespecies management programs and of man-agement/restoration programs being compro-mised by conflicts of interest. The most fa-mous case is that of invasive Tamarix speciesas a habitat for birds, in particular the endan-gered southwestern willow flycatchers (Empi-donax traillii subsp. extimus) (149). Flycatch-ers never occurred in areas now dominatedby Tamarix, but now that they are thereand are rare elsewhere, value judgments mustbe made; which do we value more, flycatch-ers or riparian ecosystems more conducive tothe sustainable delivery of key ecosystem ser-vices? Such examples point to the need formore careful consideration of all implicationsof planned control and restoration programs(150). Many control/repair/restoration effortshave unplanned and undesirable consequences.The textbook example is that of mesopredatorrelease, whereby control of a top predator, suchas cats, can lead to increased densities of in-termediate predators with effects that cascadedown through the ecosystem. This scenario,with minor variations of the plot and with dif-ferent actors, has been replayed on countlessislands following control efforts against inva-sive vertebrates (see Reference 151). The orderof removing invasive vertebrate species clearlymatters (152). The overall cause for such prob-lems is that invasive species are increasingly in-filtrating various networks, notably pollinationand dispersal networks and food webs, wherethey forge novel functions (28, 153). When theyare removed without due consideration of pre-vailing functions and interactions, rapid col-lapses may and do occur. Given the increas-ing extent and abundance of invasive speciesworldwide, such issues will become much morecommon (154, 155).


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Novel Ecosystems: Refocusingon Management Targets

The escalating scale of biological invasions andsynergies between invasive species and otherfacets of global change generating greater andincreasingly complex influences on ecosystems(155) are increasingly causing many problemsfor restoration ecologists. Among the prob-lems are those relating to defining and select-ing meaningful and appropriate reference sitesor targets for restoration (e.g., Reference 156).It is becoming increasingly obvious in manyecosystems, especially those with high levels ofhuman influence, that restoration of habitatsdegraded by invasive species to some pristinecondition is both futile and impractical or im-possible (157). This is because invasive speciesthemselves often alter ecosystems to the ex-tent that preclude many native species or flour-ish as a symptom of changes driven by othercauses.

There is increasing support for a revision ofconservation and restoration strategies to em-brace the notion of “novel ecosystems”—thosecomprising species that occur in combinationsand relative abundances that have not occurredpreviously at a given location or biome. Suchnovel ecosystems result from the degradationor invasion of native or wild ecosystems or theabandonment of intensively managed systems(158, 159). Examples include formation ofmixed communities of evergreen broad-leavedplants established in areas previously occupiedby deciduous broad-leaved forests at the south-ern foot of the European Alps as a result ofclimate warming (160) and the reorganized ma-rine ecosystems of the Atlantic Ocean (161) andMediterranean Sea (162). Such communitiesraise many important applied questions, in-cluding those about elucidating the factors thatenable native species to persist with invaders.Because these ecosystems are the result of de-liberate or inadvertent human action and theirkey novel feature is the potential for changesin ecosystem functioning, consideration needsto be given to developing appropriate man-agement goals and approaches under new

conditions (158). This may involve viewingthe role of aliens more pragmatically in thecontext of shifting species’ ranges and changingcommunities and even considering some newspecies as key (desirable) elements for maintain-ing ecosystem services (154). Removing alienspecies from such, often human-dominated,systems is often impractical, and managementis sometimes (but not always) more effectivelydirected at managing these novel ecosystemsto provide sustainable delivery of certainfunctions or services. Therefore, among themany challenges facing invasion biologists andrestoration ecologists is the need to confrontrapidly “changing perceptions of change”(163).

CONCLUSIONS� Invasive species are increasing in num-

ber, extent, and influence worldwide.They are both passengers (symptoms)and drivers of change, and they interactsynergistically with many other facets ofglobal change. In many cases they causerapid and dramatic ecosystem degrada-tion, loss of biodiversity, and homoge-nization of regional biotas. Many other,more subtle effects also have profound(usually negative) implications.

� Invasion ecology has exploded as a field ofstudy, and thousands of publications aregenerated every year on an increasinglybroad range of themes. Scientific studiesfocusing on impacts and practical solu-tions to problems caused by invasions ini-tially lagged behind case studies and thosedescribing and elucidating biogeograph-ical patterns and ecological mechanismsbut are now becoming well representedin the literature.

� There are marked geographical and tax-onomical biases in the study of inva-sions and invasive species, but there havebeen major advances in the understand-ing of invasions for most taxonomicgroups and major biomes in recent years.New technologies, notably molecular


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methods, remote sensing, and comput-ers, have radically improved our ability toassemble accurate inventories, map andmodel distributions and the effect of in-terventions, and explore patterns of inva-sive species. Such insights are improvingour ability to plan, assess, and monitorcontrol operations.

� The harmful effects of invasive species arerecognized in many parts of the worldand integrated strategies have been im-plemented to reduce current and fu-ture impacts. We have reviewed ex-citing developments in risk assessment,pathway management, early detectionand rapid response, and mitigation andrestoration.

� Multiple facets of global change pose sig-nificant challenges for ecologists and con-servation biologists, and new approachesare needed for managing biodiversity.Every effort should be made to keep rep-resentative areas, such as protected ar-eas, free of alien species. However, inthe increasingly human-dominated ma-trix, more pragmatic approaches will beneeded. For example, management mayin many cases be more effectively directedtoward building and maintaining ecosys-tems capable of delivering key ecosys-tem services than attempting to steer de-graded ecosystems back to some historicpristine, alien-free condition, which maybe futile.

SUMMARY POINTS

1. Invasive species are increasing in number, extent, and influence worldwide as a result ofincreasing globalization.

2. Harmful ecological effects of biological invasions are recognized in many parts of theworld. Invasive species cause rapid and dramatic ecosystem degradation, loss of biodi-versity, and homogenization of regional biotas, and they impact on ecosystem servicesand on human health and well-being.

3. Translation of ecological effects of biological invasions into monetary terms is still in itsinfancy, but the limited data available point to invasive species incurring huge economiccosts in many sectors, notably agriculture, forestry, fisheries, aquaculture, the pet trade,and nature conservation.

4. Understanding of the ecological consequences of biological invasions is improving, butbetter metrics for quantifying impacts must be developed and applied to allow for theobjective prioritization of species to help in prioritizing action and to facilitate the transferof information between regions.

5. Invasion ecology is profiting from its interlinkage with other disciplines such as conser-vation biology, restoration ecology, global change biology, and reintroduction ecology,but better integration of ecological perspectives with socioeconomic considerations isessential.

6. Rapid development of new technologies has improved our ability to assess, monitor,and plan control operations, and integrated strategies are starting to be implemented toreduce current and future impacts of invasive species. Biosecurity policies and strategiesmust be updated regularly to capitalize on new findings.


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7. Management needs to focus on early stages of the invasion process for which recent de-velopments in risk assessment, pathway and vector management, and early detection andrapid response provide a solid foundation; prevention is more effective than mitigationand restoration after invasion has taken place.

8. More pragmatic approaches have to be considered in some situations. For example, insome cases, management may be most efficiently directed toward building and maintain-ing novel ecosystems capable of delivering key ecosystem services, rather than attemptingto restore degraded ecosystems to alien-free conditions.

FUTURE ISSUES

1. Invasion ecology is rapidly becoming interlinked and interweaved with other disci-plines, such as conservation biology, restoration ecology, global change biology, andreintroduction ecology. New frameworks are required for integrating insights from dis-parate disciplines, for example, to integrate ecological perspectives with socioeconomicconsiderations.

2. Better metrics are needed for quantification of impacts to allow for the objective pri-oritization of species for action and to facilitate the transfer of information betweenregions.

3. Biosecurity policies and strategies are being implemented without adequate conceptual-ization and verification of keystone assumptions. Every aspect of such policies needs tobe researched with a view to improving their scientific underpinnings.

4. Among the many pressing questions for research associated with the repair of ecosystemsfollowing the removal of invasive species are those relating to legacy effects, secondaryinvasions, and predicting ecosystem responses to different forms of manipulation. Pos-sibilities for managing some invaded systems most effectively as novel ecosystems needcareful consideration.

DISCLOSURE STATEMENT

The authors are not aware of any affiliations, memberships, funding, or financial holdings thatmight be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS

This review resulted partly from research carried out on EU-funded projects PRATIQUE (KBBE-212459), ALARM (GOCECT-2003-506675), and DAISIE (contract no. SSPI-CT-2003-511202),and it was supported by long-term research plans AV0Z60050516 from the Academy of Sciences ofthe Czech Republic, MSM0021620828 and grant LC06073 (both from the Ministry of Education,Youth and Sports of the Czech Republic) to P.P. D.M.R. acknowledges support from the DST-NRF Center of Excellence for Invasion Biology; the National Research Foundation, South Africa;and the Hans Sigrist Foundation. We thank Pam Matson for comments on the manuscript, andMontserrat Vila, Zuzana Sixtova, and Jan Pergl for assistance.


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121. Dehnen-Schmutz K, Touza J, Perrings C, Williamson M. 2007. A century of the ornamental plant tradeand its impact on invasion success. Divers. Distrib. 13:527–34

122. Foxcroft LC, Richardson DM, Wilson JRU. 2008. Ornamental plants as invasive aliens: problems andsolutions in Kruger National Park, South Africa. Environ. Manag. 41:32–51

123. Gosper CR, Vivian-Smith G. 2009. Approaches to selecting native plant replacements for fleshy-fruitedinvasive species. Restor. Ecol. 17:196–204

124. Drake JM, Lodge DM. 2004. Global hot spots of biological invasions: evaluating options for ballast-watermanagement. Proc. R. Soc. Lond. Ser. B 271:575–80

125. Presents the firstquantitative estimatesof propagule pressureassociated with aspecific introductionpathway.125. Lee JE, Chown SL. 2009. Breaching the dispersal barrier to invasion: quantification and man-

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126. Wilson JRU, Dormontt EE, Prentis PJ, Lowe AJ, Richardson DM. 2009. Something in the way youmove: Dispersal pathways affect invasion success. Trends Ecol. Evol. 24:136–44

127. Koger CH, Shaw DR, Reddy KN, Bruce LM. 2004. Detection of pitted morningglory (Ipomoea lacunosa)with hyperspectral remote sensing. II. Effects of vegetation ground cover and reflectance properties.Weed Sci. 52:230–35

128. Barnett DT, Stohlgren TJ, Jarnevich CS, Chong GW, Ericson JA, et al. 2007. The art and science ofweed mapping. Environ. Monit. Assess. 132:235–52

129. Hayes KR, Cannon R, Neil K, Inglis G. 2005. Sensitivity and cost considerations for the detection anderadication of marine pests in ports. Mar. Pollut. Bull. 50:823–34

130. Ibanez I, Silander JA, Allen JM, Treanor SA, Wilson A. 2009. Identifying hotspots for plant invasionsand forecasting focal points of further spread. J. Appl. Ecol. 46:1219–28

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132. Crall AW, Newman GJ, Stohlgren TJ, Jarnevich CS, Evangelista P, Geuenther D. 2006. Evaluatingdominance as a component of non-native species invasions. Divers. Distrib. 12:195–204

133. D’Antonio CM, Jackson NE, Horvitz CC, Hedberg R. 2004. Invasive plants in wildland ecosystems:merging the study of invasion processes with management needs. Front. Ecol. Environ. 2:513–21

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135. Meyerson LA, Reaser JK. 2003. Bioinvasions, bioterrorism, and biosecurity. Front. Ecol. Environ. 1:307–14

136. Mehrhoff LJ, Silander JA Jr, Leicht SA, Mosher ES, Tabak NM. 2003. IPANE: Invasive plant atlas ofNew England. Dept. Ecol. Evol. Biol., Univ. Conn., Storrs, CT. http://www.ipane.org

137. Smith GF, Figueiredo E. 2009. Capacity building in taxonomy and systematics. Taxon 58:697–99138. Suggests thateradication is feasiblemore often than isreflected in the currentliterature.

138. Simberloff D. 2009. We can eliminate invasions or live with them: successful managementprojects. Biol. Invasions 11:149–57

139. Courchamp F, Chapuis J-L, Pascal M. 2003. Mammal invaders on islands: impact, control and controlimpact. Biol. Rev. 78:347–83

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141. Shows thatsuccessful eradication isunlikely above certaininfestation threshold.

141. Rejmanek M, Pitcairn MJ. 2002. When is eradication of exotic pest plants a realistic goal? InTurning the Tide: the Eradication of Invasive Species, ed. CR Veitch, MN Clout, pp. 249–53. Gland,Switz./Cambridge, UK: IUCN

142. Gardener MR, Atkinson R, Renteria JL. 2010. Eradications and people: lessons from the plant eradicationprogram in Galapagos. Restor. Ecol. 18:20–29

143. Regan TJ, McCarthy MA, Baxter PWJ, Panetta FD, Possingham HP. 2006. Optimal eradication: whento stop looking for an invasive plant. Ecol. Lett. 9:759–66

144. Holmes PM, Richardson DM, van Wilgen BW, Gelderblom C. 2000. Recovery of South African fynbosvegetation following alien woody plant clearing and fire: implications for restoration. Austral Ecol. 25:631–39

145. Zavaleta E, Hobbs RJ, Mooney HA. 2001. Viewing invasive species removal in a whole-ecosystemcontext. Trends Ecol. Evol. 16:454–59

146. Loo SE, Mac Nally R, O’Dowd DJ, Lake PS. 2009. Secondary invasions: implications of riparian restora-tion for in-stream invasion by an aquatic grass. Restor. Ecol. 17:378–85

147. Malcolm GM, Bush DS, Rice SK. 2008. Soil nitrogen conditions approach preinvasion levels followingrestoration of nitrogen-fixing black locust (Robinia pseudoacacia) stands in a pine-oak ecosystem. Restor.Ecol. 16:70–78

148. Wolfe BE, Klironomos JN. 2005. Breaking new ground: soil communities and exotic plant invasion.BioScience 55:477–87

149. Sogge MK, Sferra SJ, Paxton EH. 2008. Tamarix as habitat for birds: implications for riparian restorationin the southwestern United States. Restor. Ecol. 16:146–54


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151. Bergstrom DM, Lucieer A, Kiefer K, Wasley J, Belbin L, et al. 2009. Indirect effects of invasive speciesremoval devastate World Heritage island. J. Appl. Ecol. 46:73–81

152. Collins PW, Latta BC, Roemer GW. 2009. Does the order of invasive species removal matter? The caseof the eagle and the pig. PLoS ONE 4:e7005

153. Vila M, Bartomeus I, Dietzsch AC, Petanidou T, Steffan-Dewenter I, et al. 2009. Invasive plant integra-tion into native plant-pollinator networks across Europe. Proc. R. Soc. Lond. Ser. B 276:3887–93

154. Walther GR, Roques A, Hulme PE, Sykes M, Pysek P, et al. 2009. Alien species in a warmer world: risksand opportunities. Trends Ecol. Evol. 24:686–93

155. Schweiger O, Biesmeijer JC, Bommarco R, Hickler T, Hulme PE, et al. 2010. Multiple stressors onbiotic interactions: How climate change and alien species interact to affect pollination. Biol. Rev. 85:doi: 10.1111/j.1469-185X.2010.00125

156. Holmes PM, Richardson DM, Esler KJ, Witkowski ETF, Fourie S. 2005. A decision-making frameworkfor restoring riparian zones degraded by invasive alien plants in South Africa. S. Afr. J. Sci. 101:553–64

157. Richardson DM, Holmes PM, Esler KJ, Galatowitsch SM, Stromberg JC, et al. 2007. Riparian vegeta-tion: degradation, alien plant invasions, and restoration prospects. Divers. Distrib. 13:126–39

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162. Occhipinti-Ambrogi A. 2007. Global change and marine communities: alien species and climate change.Mar. Pollut. Bull. 55:342–52

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164. Nentwig W, ed. 2007. Biological Invasions. Berlin: Springer


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Invasion ecology

Reintroductionecology

Managed relocation (assisted

migration)

Conservationbiology

Restorationecology

Globalchangebiology

Habitat disturbance

Habitat fragmentation

Habitat destruction

Overexploitation

Pollution

Climate change Abatement policies

Protected areas

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Strategies for sustainable use

Alien species

Disciplines Factors affecting biodiversity

Loss of pollinators

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ecosystem services

Species extinctions/ loss of keystone functions/altered

ecosystem services

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National conservation

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Figure 1Invasion ecology has emerged as a discrete field, partly in response to the escalating level of threat that invasive species pose to globalbiodiversity together with other factors. The field of invasion ecology is increasingly drawing insights from (and lending some to) otherdisciplines that have themselves evolved in response to challenges in biodiversity conservation.

www.annualreviews.org • Management of Biological Invasions C-1

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ENVIRONMENTAL (LOCAL)

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C-2 Pysek · Richardson

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EG35-FM ARI 18 September 2010 7:49

Annual Review ofEnvironmentand Resources

Volume 35, 2010 Contents

Preface � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �v

Who Should Read This Series? � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �vii

I. Earth’s Life Support Systems

Human Involvement in Food WebsDonald R. Strong and Kenneth T. Frank � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 1

Invasive Species, Environmental Change and Management, and HealthPetr Pysek and David M. Richardson � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �25

Pharmaceuticals in the EnvironmentKlaus Kummerer � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �57

II. Human Use of Environment and Resources

Competing Dimensions of Energy Security: An InternationalPerspectiveBenjamin K. Sovacool and Marilyn A. Brown � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �77

Global Water Pollution and Human HealthRene P. Schwarzenbach, Thomas Egli, Thomas B. Hofstetter, Urs von Gunten,

and Bernhard Wehrli � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 109

Biological Diversity in Agriculture and Global ChangeKarl S. Zimmerer � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 137

The New Geography of Contemporary Urbanization and theEnvironmentKaren C. Seto, Roberto Sanchez-Rodrıguez, and Michail Fragkias � � � � � � � � � � � � � � � � � � � � � 167

Green Consumption: Behavior and NormsKen Peattie � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 195

viii

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EG35-FM ARI 18 September 2010 7:49

III. Management, Guidance, and Governance of Resources and Environment

Cities and the Governing of Climate ChangeHarriet Bulkeley � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 229

The Rescaling of Global Environmental PoliticsLiliana B. Andonova and Ronald B. Mitchell � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 255

Climate RiskNathan E. Hultman, David M. Hassenzahl, and Steve Rayner � � � � � � � � � � � � � � � � � � � � � � � � � 283

Evaluating Energy Efficiency Policies with Energy-Economy ModelsLuis Mundaca, Lena Neij, Ernst Worrell, and Michael McNeil � � � � � � � � � � � � � � � � � � � � � � � � � 305

The State of the Field of Environmental HistoryJ.R. McNeill � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 345

Indexes

Cumulative Index of Contributing Authors, Volumes 26–35 � � � � � � � � � � � � � � � � � � � � � � � � � � � 375

Cumulative Index of Chapter Titles, Volumes 26–35 � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 379

Errata

An online log of corrections to Annual Review of Environment and Resources articles maybe found at http://environ.annualreviews.org

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Documents

Invasive Species, Environmental Change and Management, and ...faculty.washington.edu/wgold/BES301/invasive... · EG35CH02-Pysek ARI 18 September 2010 6:55 Invasive Species, Environmental