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REVIEW / SYNTHÈSE Effects of climate change on the distribution of invasive alien species in Canada: a knowledge synthesis of range change projections in a warming world Andrea L. Smith, Nina Hewitt, Nicole Klenk, Dawn R. Bazely, Norman Yan, Stepan Wood, Irene Henriques, James I. MacLellan, and Carla Lipsig-Mummé Abstract: The interactive effects of climate change and invasive alien species (IAS) pose serious threats to biodiversity, eco- systems and human well-being worldwide. In particular, IAS are predicted to experience widespread changes in distribution in response to climate change, with many expanding their ranges into new areas. However, the two drivers of global change are seldom considered together in policy and management. We conducted a knowledge synthesis to assess the state of re- search on IAS range shifts under climate change in Canada. We found that the study of IAS distribution changes caused by climate change is a relatively new field of inquiry that integrates research in the areas of ecology, conservation biology, and environmental sciences. The multidisciplinary dimensions of the issue are largely overlooked in the scholarly literature, with most studies having a purely natural science perspective. Very little original research has occurred in the field to date; in- stead literature reviews are common. Research focuses on modeling range changes of current IAS threats, rather than pre- dicting potential future IAS threats. The most commonly studied IAS already occur in Canada as native species that have spread beyond their range (e.g., lyme disease, mountain pine beetle, smallmouth bass) or as established invaders (e.g., gypsy moth). All of these IAS are expected to expand northward with climate change, resulting in widespread negative impacts on forest and freshwater biodiversity, carbon sequestration, and public health. Many barriers to predicting IAS range change under climate change are identified in the literature, including the complexity of the issue, lack of ecological data, and fail- ure to integrate climate change IAS interactions into research, policy, and management. Recommendations for increased research and monitoring, and the need for policy and management reform predominate in the literature. Key words: climate change, invasive alien species, range, distribution, knowledge synthesis, global change. Résumé : Les effets interactifs du changement climatique et des espèces adventices envahissantes (EAE) constituent des me- naces sérieuses à la biodiversité, aux écosystèmes et au bien-être des humains. De façon plus précise, on prédit que les EAE connaitront des modifications générales de leur distribution en réaction au changement climatique, plusieurs dentre elles étendant leur aire dans de nouvelles régions. Cependant, on considère rarement simultanément ces deux responsables du changement global dans les politiques et laménagement. Les auteurs ont effectué une synthèse des connaissances pour éva- luer létat de la recherche sur les déplacements des aires de distribution des EAE causés par le changement climatique, au Received 10 May 2011. Accepted 20 September 2011. Published at www.nrcresearchpress.com/er on 19 January 2012. A.L. Smith,* D.R. Bazely, and N. Yan. Institute for Research and Innovation in Sustainability (IRIS), York University, 4700 Keele St., Toronto, ON M3J 1P3, Canada; Department of Biology, York University, 4700 Keele St., Toronto, ON M3J 1P3, Canada. N. Hewitt. Institute for Research and Innovation in Sustainability (IRIS), York University, 4700 Keele St., Toronto, ON M3J 1P3, Canada; Department of Geography, York University, 4700 Keele St., Toronto, ON M3J 1P3, Canada. N. Klenk. Institute for Research and Innovation in Sustainability (IRIS), York University, 4700 Keele St., Toronto, ON M3J 1P3, Canada. S. Wood. Institute for Research and Innovation in Sustainability (IRIS), York University, 4700 Keele St., Toronto, ON M3J 1P3, Canada; Osgoode Hall Law School, York University, 4700 Keele St., Toronto, ON M3J 1P3, Canada; Robert Schuman Centre for Advanced Studies, European University Institute, San Domenico di Fiesole 50014, Italy. I. Henriques. Institute for Research and Innovation in Sustainability (IRIS), York University, 4700 Keele St., Toronto, ON M3J 1P3, Canada; Schulich School of Business, York University, 4700 Keele St., Toronto, ON M3J 1P3, Canada. J.I. MacLellan. Institute for Research and Innovation in Sustainability (IRIS), York University, 4700 Keele St., Toronto, ON M3J 1P3, Canada; Faculty of Environmental Studies, York University, 4700 Keele St., Toronto, ON M3J 1P3, Canada. C. Lipsig-Mummé. Institute for Research and Innovation in Sustainability (IRIS), York University, 4700 Keele St., Toronto, ON M3J 1P3, Canada; Department of Social Science, York University, 4700 Keele St, Toronto, ON M3J 1P3, Canada. Corresponding author: Andrea L. Smith (e-mail: [email protected]). *Present address: Department of Biology, York University, 4700 Keele St., Toronto, ON M3J 1P3, Canada. 1 Environ. Rev. 20:116 (2012) doi:10.1139/A11-020 Published by NRC Research Press Environ. Rev. Downloaded from www.nrcresearchpress.com by 99.233.36.227 on 01/21/12 For personal use only.
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Page 1: Effects of climate change on the distribution of invasive alien species in Canada: a knowledge synthesis of range change projections in a warming world

REVIEW / SYNTHÈSE

Effects of climate change on the distribution ofinvasive alien species in Canada: a knowledgesynthesis of range change projections in awarming world

Andrea L. Smith, Nina Hewitt, Nicole Klenk, Dawn R. Bazely, Norman Yan,Stepan Wood, Irene Henriques, James I. MacLellan, and Carla Lipsig-Mummé

Abstract: The interactive effects of climate change and invasive alien species (IAS) pose serious threats to biodiversity, eco-systems and human well-being worldwide. In particular, IAS are predicted to experience widespread changes in distributionin response to climate change, with many expanding their ranges into new areas. However, the two drivers of global changeare seldom considered together in policy and management. We conducted a knowledge synthesis to assess the state of re-search on IAS range shifts under climate change in Canada. We found that the study of IAS distribution changes caused byclimate change is a relatively new field of inquiry that integrates research in the areas of ecology, conservation biology, andenvironmental sciences. The multidisciplinary dimensions of the issue are largely overlooked in the scholarly literature, withmost studies having a purely natural science perspective. Very little original research has occurred in the field to date; in-stead literature reviews are common. Research focuses on modeling range changes of current IAS threats, rather than pre-dicting potential future IAS threats. The most commonly studied IAS already occur in Canada as native species that havespread beyond their range (e.g., lyme disease, mountain pine beetle, smallmouth bass) or as established invaders (e.g., gypsymoth). All of these IAS are expected to expand northward with climate change, resulting in widespread negative impacts onforest and freshwater biodiversity, carbon sequestration, and public health. Many barriers to predicting IAS range changeunder climate change are identified in the literature, including the complexity of the issue, lack of ecological data, and fail-ure to integrate climate change – IAS interactions into research, policy, and management. Recommendations for increasedresearch and monitoring, and the need for policy and management reform predominate in the literature.

Key words: climate change, invasive alien species, range, distribution, knowledge synthesis, global change.

Résumé : Les effets interactifs du changement climatique et des espèces adventices envahissantes (EAE) constituent des me-naces sérieuses à la biodiversité, aux écosystèmes et au bien-être des humains. De façon plus précise, on prédit que les EAEconnaitront des modifications générales de leur distribution en réaction au changement climatique, plusieurs d’entre ellesétendant leur aire dans de nouvelles régions. Cependant, on considère rarement simultanément ces deux responsables duchangement global dans les politiques et l’aménagement. Les auteurs ont effectué une synthèse des connaissances pour éva-luer l’état de la recherche sur les déplacements des aires de distribution des EAE causés par le changement climatique, au

Received 10 May 2011. Accepted 20 September 2011. Published at www.nrcresearchpress.com/er on 19 January 2012.

A.L. Smith,* D.R. Bazely, and N. Yan. Institute for Research and Innovation in Sustainability (IRIS), York University, 4700 Keele St.,Toronto, ON M3J 1P3, Canada; Department of Biology, York University, 4700 Keele St., Toronto, ON M3J 1P3, Canada.N. Hewitt. Institute for Research and Innovation in Sustainability (IRIS), York University, 4700 Keele St., Toronto, ON M3J 1P3, Canada;Department of Geography, York University, 4700 Keele St., Toronto, ON M3J 1P3, Canada.N. Klenk. Institute for Research and Innovation in Sustainability (IRIS), York University, 4700 Keele St., Toronto, ON M3J 1P3, Canada.S. Wood. Institute for Research and Innovation in Sustainability (IRIS), York University, 4700 Keele St., Toronto, ON M3J 1P3, Canada;Osgoode Hall Law School, York University, 4700 Keele St., Toronto, ON M3J 1P3, Canada; Robert Schuman Centre for AdvancedStudies, European University Institute, San Domenico di Fiesole 50014, Italy.I. Henriques. Institute for Research and Innovation in Sustainability (IRIS), York University, 4700 Keele St., Toronto, ON M3J 1P3,Canada; Schulich School of Business, York University, 4700 Keele St., Toronto, ON M3J 1P3, Canada.J.I. MacLellan. Institute for Research and Innovation in Sustainability (IRIS), York University, 4700 Keele St., Toronto, ON M3J 1P3,Canada; Faculty of Environmental Studies, York University, 4700 Keele St., Toronto, ON M3J 1P3, Canada.C. Lipsig-Mummé. Institute for Research and Innovation in Sustainability (IRIS), York University, 4700 Keele St., Toronto, ON M3J 1P3,Canada; Department of Social Science, York University, 4700 Keele St, Toronto, ON M3J 1P3, Canada.

Corresponding author: Andrea L. Smith (e-mail: [email protected]).

*Present address: Department of Biology, York University, 4700 Keele St., Toronto, ON M3J 1P3, Canada.

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Environ. Rev. 20: 1–16 (2012) doi:10.1139/A11-020 Published by NRC Research Press

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Canada. Ils ont constaté que l’étude des modifications de la distribution des EAE causées par le changement climatiqueconstitue un champ de recherche relativement nouveau, intégrant les travaux dans les domaines de l’écologie, de la biologiede conservation et des sciences de l’environnement. Dans la littérature scientifique, on sous-estime largement les dimensionsmultidisciplinaires, la plupart des études étant conduites dans une perspective purement de sciences naturelles. On observetrès peu de recherche originale dans ce domaine à ce jour, alors qu’on trouve de nombreuses revues de littérature. La recher-che se concentre sur la modélisation des modifications d’aire des menaces actuelles venant des EAE, plutôt que la prédictiondu potentiel futur des menaces venant des EAE. Les études les plus fréquentes sur les EAE concernent des espèces indigè-nes qui se sont répandues au-delà de leur aire (p.ex. maladie de lyme, dendroctone du pin, achigan à petite bouche) des en-vahisseurs établis (p. ex. la spongieuse). On s’attend à ce que toutes ces EAE se répandent vers le Nord sous l’influence duchangement climatique, entrainant d’importants effets négatifs sur la biodiversité des forêts et des milieux d’eau douce, laséquestration du carbone et la santé publique. À partir de la littérature, on identifie plusieurs barrières à la prédiction deschangements d’aire des EAE sous l’influence du changement climatique, incluant la complexité de la question, le manquede données écologiques et l’échec de l’intégration des interactions entre les EAE et le climat en recherche, politique et enaménagement. Les auteurs recommandent l’augmentation de la recherche et du suivi ainsi que le besoin qu’une réforme po-litique/aménagement prédomine dans la littérature.

Mots‐clés : changement climatique, espèces adventices envahissantes, aire, distribution, synthèse des connaissances, change-ment global.

[Traduit par la Rédaction]

Introduction

Climate change and invasive alien species (IAS) are widelyrecognized as pressing environmental and socio-economic is-sues worldwide. Despite mounting evidence that these majordrivers of global change have strong and complex connec-tions with each other, climate change and IAS are typicallytreated as independent problems, and their interactions areignored in policy and management initiatives (Pyke et al.2008; Walther et al. 2009). At a time when the effects of cli-mate change and IAS are steadily increasing globally, failureto address their dynamic linkages will only exacerbate nega-tive impacts on the environment, economy, and society.Climate change and IAS are linked in many ways. IAS are

any organisms that are moved beyond their previous range byhuman agency, either deliberately or accidentally, and thatcause environmental and (or) socio-economic harm in theirnew surroundings (McNeely 2001). Climate change, and so-cietal responses to it, are likely to intensify the impacts ofIAS at all stages of the invasion process, by providing in-creased opportunities for IAS to cross historical geographicbarriers, and to establish and spread in new areas (Walther etal. 2009). At the same time, IAS may influence the magni-tude, rate, and impact of climate change by altering ecosys-tem structure and function (e.g., by changing fire cycles andresidence times of carbon sinks; Pyke et al. 2008). Climatechange and IAS could increasingly interact in a positive feed-back loop, with climate change opening up new habitat forIAS, and IAS subsequently making ecosystems more suscep-tible to climate change (McNeely 2000).Climate change is expected to have profound effects on

IAS dynamics worldwide. Changing patterns of human trans-port (e.g., new trade routes, or ones that are open more of thetime) will enhance opportunities for potential and current in-vaders to reach new destinations and will lead to increasedsurvival rates (Hellmann et al. 2008). Opening of the North-west Passage to shipping, for example, could introduce amyriad of nonnative species to the Canadian arctic (Mainkaand Howard 2010). This new trading route will also reduce

transit times, potentially increasing survival of biofouling orballast-water organisms (Pyke et al. 2008). Changing climateconditions will mean that species once unable to persist incertain areas because of physiological constraints will nowsurvive and colonize successfully. Consequently, the distribu-tion of many IAS currently limited by cold temperatures willlikely expand (although some IAS ranges may also contractdue to warming temperatures (Bradley et al. 2010a). ManyIAS thrive in disturbed habitats, which will become morecommon as a result of rising temperatures, increased fire out-breaks, and more severe and frequent extreme weather eventsexpected under climate change (McNeely 2000). IAS alsowill benefit from new niches becoming available if nativespecies are no longer adapted to changing climate conditions(McNeely 2000). IAS impacts undoubtedly will be altered byclimate change, and the effectiveness of current managementstrategies could diminish (Chornesky and Randall 2003). Forexample, some terrestrial IAS plants may become resistant toexisting herbicides under increasing CO2 levels associatedwith climate change (Hellmann et al. 2008). Combined withaccelerating trade liberalization, tourism, and habitat destruc-tion occurring globally, climate change thus is likely to sig-nificantly increase the rate and extent of biological invasionsaround the world (McNeely 2000; Sutherst 2000; Walther etal. 2009).The serious threats posed by the interaction of climate

change and IAS are gradually being recognized by the scien-tific community (e.g., Sutherst 2000; Hellmann et al. 2008;Walther et al. 2009; Fleishman et al. 2011). The Intergovern-mental Panel on Climate Change (IPCC) covers the issue inconsiderable detail in its most recent assessment report(IPCC 2007). The report links recent warming worldwidewith poleward and altitudinal shifts in plant and animalranges and forecasts that many ecosystems will become vul-nerable to biological invasions as climatic barriers are re-moved. The IPCC concludes that a temperature increase ofgreater than 1.5 °C–2.5 °C of the global average temperaturewill cause dramatic changes to species distributions and eco-system structure and function, resulting in overwhelmingly

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negative consequences for global biodiversity and ecosystemgoods and services (IPCC 2007). In Canada, such a rise intemperature could lead to both new species expanding theirranges into the country from southern origins (e.g., from theUS; Noss et al. 2009) and existing species expanding theirranges within the country (e.g., mountain pine beetle (Den-droctonus ponderosae); Chiotti and Lavender 2008). In bothcases, the potential for IAS to spread into new areas is high.Arctic Canada, in particular, is predicted to experience pro-found ecological changes as a result of dramatic climatewarming, including northward migrations of southern spe-cies, the emergence of new infectious diseases, and the dis-placement of tundra by boreal forest (Ford and Smit 2004;Prowse et al. 2009).The significance of the link between climate change and

IAS has yet to be reflected in policy or legislation, at leastin North America. Indeed, a recent review of US policy re-vealed that neither climate change nor IAS policy explicitlyaddresses the issue of their interaction (Pyke et al. 2008).The US Environmental Protection Agency published a reportin 2008 predicting future introductions of IAS to the GreatLakes, without any mention of the impact of climate changeon IAS arrival or subsequent colonization (USEPA 2008).Response to the problem is similarly lacking in Canada.

Although climate change – IAS interactions are acknowl-edged in recent federal government reports on projected cli-mate change impacts, risks, and adaptation strategies(Lemmen and Warren 2004; Lemmen et al. 2008a), theseconcerns have not been translated into concrete policy or ac-tion on the issue. Federal documents acknowledge that IASare expected to increase and spread northward in Canadaunder climate change. Furthermore, the connection betweenclimate change and IAS is identified as a knowledge gap re-quiring study (Lemmen et al. 2008a). Yet the federal govern-ment’s An Invasive Alien Species Strategy for Canada,completely overlooks the question of climate change andIAS (Government of Canada 2004). In a 2008 report to par-liament, the Auditor General of Canada noted that the federalgovernment has failed to develop priorities or objectives forthe prevention, control, and eradication of aquatic IAS, andlacks plans for early detection and rapid response. Further-more, the government does not measure or report on the ef-fectiveness of federal efforts to manage aquatic IAS (Officeof the Auditor General 2008). The situation at the provinciallevel is no better, with little to no mention of the issue, forexample, in New Brunswick’s action plan on climate change(Government of New Brunswick 2007), Ontario’s action planon climate change (Government of Ontario 2007), or BritishColumbia’s IAS strategy (Government of British Columbia2004).Climate change is already altering environmental condi-

tions across Canada. Much of the country is experiencing in-creased average annual temperatures, affecting precipitationpatterns, climate variability, and the frequency and intensityof extreme weather events (Lemmen et al. 2008b). The result-ing disruption of native ecosystems, coupled with risingglobalization, provides enriched opportunities for establishedIAS to spread into new areas, and potential IAS to be intro-duced into Canada. Predicting the distribution changes of ex-isting and potential IAS under climate change, and

understanding their anticipated impacts, is critical if we areto effectively manage IAS in Canada in the future.In this synthesis we examine the state of knowledge on

IAS range shifts under climate change in Canada. Our studyencompasses distribution changes of both current IAS inCanada, and potential IAS not yet in the country (i.e., speciesknown to be invasive elsewhere that could potentially invadeCanada) as a result of a changing climate. These types ofIAS may include species that are native to parts of NorthAmerica, but have become invasive in other regions of thecontinent as a result of human activity (e.g., smallmouthbass (Micropterus dolomieu); Sharma et al. 2009a), as wellas nonindigenous species introduced to North America thathave become invasive here (e.g., zebra mussel (Dreissenapolymorpha); Drake and Bossenbroek 2004). NonIAS spe-cies are not a focus of the research (e.g., alien species withno known negative impacts).We explore coverage of the issue in the primary literature

to identify (i) known or projected IAS range changes underclimate change; (ii) documented or anticipated impacts ofthese range changes; (iii) barriers to reliable range changeprojections; and (iv) recommendations for addressing the in-teractive effects of climate change and IAS. We also charac-terize the structure and dynamics of research in the fieldthrough a bibliometric analysis. By documenting the extentand nature of scholarly attention given to climate change andIAS in Canada, we seek to explore possible reasons for theabsence of government policy on the issue in Canada. Forexample, lack of policy might reflect a lack of scholarly re-search. Alternatively, it might indicate that linkages are notbeing made between complementary, but isolated, researchdomains, such as climate change science and invasion biol-ogy. We believe such an exercise is an important first steptoward developing policy and action on the emerging threatof IAS range shifts caused by climate change. To our knowl-edge, this is the first such synthesis of the literature on cli-mate change and IAS in a Canadian context.

MethodsWe conducted a knowledge synthesis to assess the current

state of knowledge on the subject of IAS range shifts underclimate change in Canada. The purpose of a knowledge syn-thesis is to examine scholarly literature in two or more re-search domains so that complementary knowledge on aparticular topic can be unified (Sneed 2003). The knowledgesynthesis approach typically consists of a structured literaturesearch combined with bibliometric analysis. In this way,knowledge syntheses describe both the content of the litera-ture, and its structure and dynamics (e.g., publication pat-terns, methodological and focal trends; Janssen 2007; Triccoet al. 2010). Knowledge syntheses are thus able to reveal notonly the nature of scholarly knowledge on a topic, but alsowhere gaps exist in how that knowledge is being generated.Our knowledge synthesis consists of two parts: a literature re-view and a bibliometric analysis.For the literature review, we surveyed existing published

primary literature from the natural sciences, social sciences,and humanities. We conducted a literature search of projectedand observed changes to the distribution of current and po-tential IAS in Canada using three online academic citation in-

Smith et al. 3

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dices: GoogleScholar (using all subject areas), Scopus (usingLife Sciences, Health Sciences, Physical Sciences, and SocialSciences & Humanities indices) and Web of Science (usingScience Citation Index Expanded, Social Sciences CitationIndex, and Arts & Humanities Citation Index) for all years.The databases were accessed on 10, 25, 30 March; 12 April;and 6, 7 July 2010.We used the following combinations ofsearch terms:

1. Google Scholar: ‘invasive species’, ‘climate change’, ‘dis-tribution’, ‘Canada’

2. Scopus: invasive species AND distribution OR range ORspread AND climate change OR warming OR globalchange OR elevated CO2 AND Canad?

3. Web of Science: alien OR exotic OR invad* OR invasi*OR non-native OR non-indigenous OR introduc* ANDspecies AND distribution OR range OR spread AND cli-mate change OR warming OR global change OR elevatedCO2 AND Canada OR Newfoundland OR Prince EdwardIsland OR Nova Scotia OR New Brunswick OR QuebecOR Ontario OR Manitoba OR Saskatchewan OR AlbertaOR British Columbia OR Nunavut OR Northwest Terri-tories OR Yukon AND alpine OR arctic OR boreal ORGreat Lakes OR prairie OR maritimeWe reviewed the title and abstract of each article generated

in our search for relevance, and discarded any articles thatdid not match the subject matter. We organized the remainingrecords in EndNote and removed duplications. We read infull the top-ten most-cited papers overall, as well as all ar-ticles with a Canadian focus (a total of 47 papers). For allother papers, we either read the abstract (57 papers) orscanned the text if the abstract did not provide sufficient de-tail (47 papers).To characterize the Canadian primary literature on IAS

range shifts under climate change we collected informationon: (i) known or projected IAS range changes as a result ofclimate change; (ii) documented or anticipated impacts ofthese range changes; (iii) barriers to reliable range changeprojections; and (iv) recommendations for addressing the in-teractive effects of climate change and IAS.To classify recommendations made within reviewed ar-

ticles, we first grouped them into the following broad catego-ries, based on the type of action that was needed, asidentified in the literature: (i) policy/management reform; (ii)science and technological advances; (iii) monitoring; (iv) re-search; (v) changes to societal behaviour; and (vi) education.We then classified recommendations into more detailed cate-gories, based on recurring themes that emerged in the litera-ture (e.g., strengthen prevention strategies, improve modelingof spread etc.).We carried out a bibliometric analysis to characterize the

structure and dynamics of the scholarly literature by address-ing questions such as when researchers began studying thetopic, whether scholarly attention has changed over time, therelative impact of different articles in the field (e.g., to iden-tify the most influential studies), the most common researchmethods used, and the species studied most and least fre-quently. We classified articles based on the following classifi-cation scheme (MacLellan 2008):

• subject area (natural sciences, social sciences, humanities,multi-disciplinary)

• Web of Science subject area (e.g., Ecology, EnvironmentalSciences, Public Health)

• number of citations• year of publication• journal and journal impact factor• geographic focus (i.e., did the paper have a Canadian,

North American, or global/general focus?)• focus (i.e., was climate change and IAS a major focus of

the paper?)• article type (i.e., according to its coverage of projected

range change of IAS under climate change, see Table 1)• study method (e.g., field observation or experiment, simu-

lation/modeling, policy development, literature review)• sector (e.g., agriculture, forestry, health)• habitat (aquatic, terrestrial, both)• taxonomic group (e.g., mammal, bird, plant)• species

Results

A total of 247 papers were generated by our searches,which were subsequently reduced to 151 relevant papers,published in 88 journals. The majority of papers had a natu-ral science focus (80%), while 14% took a multidisciplinaryapproach (e.g., natural science and social science). Only 6%of papers represented the social sciences, and none werefound in the humanities. According to the Web of Sciencesubject categories (based on journal content), most papers ap-peared in journals classified as ‘Ecology’ (38%), followed by‘Environmental Sciences’ (23%), ‘Biodiversity Conservation’(15%), ‘Marine and Freshwater Biology’ (12%), and ‘PlantSciences’ (9%). (Note that many papers were in journals as-signed to multiple categories under the Web of Science sys-tem.) The top-ten most-cited papers were in journalsrepresented by the Web of Science categories ‘Biology’,‘Fisheries; Marine and Freshwater Biology’, ‘Water Resour-ces’, ‘Multidisciplinary Sciences’, ‘Ecology’, ‘Ecology; Envi-ronmental Sciences’ and ‘Biodiversity Conservation;Ecology; Environmental Sciences’. Six of the top-ten articlesfocused specifically on climate change and IAS (Table 2).The earliest paper found in our search was published in

1989, and few papers were published on the topic before2001 (i.e., 10 papers were published from 1989–2000 versus141 published from 2001–2010). There has been a steady in-crease in publications in the field since 1995 (Fig. 1). Mostpapers (36%) were published in 2008 and 2009. No particularjournal dominated publications in the field, but journals hav-ing several articles on the topic tended to have high impactfactors (i.e., greater than 2.0; Table 3), indicating that IAS –climate change interactions are being covered in prominentrather than obscure journals. Overall, coverage of IAS andclimate change was low in all journals. The maximum num-ber of articles on the topic published in a single journal was8, while the average number per journal was 1.7.Not surprisingly (given the geographical and ecosystem

search terms used), most of the papers focused on NorthAmerica (70%), however, only a quarter specifically ad-dressed climate change – IAS interactions within a Canadiancontext.Climate change and IAS interactions were a major focus of

72% of all papers from our search. The majority of papers

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(34%) examined the potential range shifts of current IAS underclimate change (category 1, Table 1). Only 6% of papers dis-cussed projected range shifts of potential IAS under climatechange (category 2, Table 1). When all categories of articletypes focusing on contemporary range shifts (i.e., categories1, 1b, 2, 3, 3b) were added together, 67% of papers examinedshifts under climate change. Literature reviews were the mostcommon type of paper generated by our search (42%), fol-lowed by simulation/modeling studies (27%). Field observa-tions or experiments represented only 11% of all papers, whilelab experiments represented 5%. None of the articles generatedin our search were meta-analyses of other studies.Most papers (48%) did not focus on a particular socio-

economic sector when examining IAS range shifts under cli-mate change. However, 21% of papers had a forestry perspec-tive, while 11% considered fisheries. Health and agriculturalissues were examined in 7% and 6% of papers, respectively.Of those papers that dealt with specific IAS (as opposed to

general concepts), most (58%) studied terrestrial species, fol-lowed by aquatic species (27%). Only 15% considered terres-trial and aquatic species jointly. The majority of papersfocused on IAS plants (47%) and invertebrates (42%), whileIAS microbes (19%), fish (9%), birds (2%), and mammals(1%) did not figure as prominently in the literature (note thatpercent exceeds 100 because many studies examined a vari-ety of taxa, not just one group). No particular IAS was thefocus of the majority of studies. The most commonly studiedIAS species were covered in only a small percentage of pub-lications: (i) the bacterium Borrelia burgdorferi (Lyme dis-ease) and its host the deer tick (Ixodes scapularis) (8%);mountain pine beetle (7%); smallmouth bass (7%); and gypsymoth (Lymantria dispar) (5%). All of these species currentlyoccur in Canada and have already expanded (mountain pinebeetle) or are expected to expand (i.e. Lyme disease and in-sect host; smallmouth bass; gypsy moth) their ranges as a re-sult of climate change (Table 4).

Table 1. Classification of articles according to their coverage of projected range change of IAS under climate change.

Category Article Type1 Describes potential range change of current IAS in Canada due to climate change (i.e., IAS is already established in Canada)1b Describes actual range change of current IAS in Canada due to climate change2 Describes potential range change of potential IAS under climate change (i.e., IAS is not currently in Canada but is considered

IAS elsewhere and is predicted to expand into Canada under climate change)3 Describes potential range change of nonIAS species in or into Canada under climate change (i.e., species is not currently

identified as IAS)3b Describes actual range change of nonIAS species in or into Canada due to climate change4 Mentions IAS range change as a consequence of climate change but not the main focus of the paper5 Mentions climate change and IAS but not as interacting forces6 Documents paleo-ecological range change under climate change7 Mentions climate change and range change in key words but not in text8 Mentions impacts of climate change on IAS not including range change9 Does not mention range change under climate change specifically but pertinent to study (e.g., may discuss applicable modeling

technique)

Table 2. Top-ten most-cited articles on IAS range change and climate change.

Times cited Author (Year) Title Journal181 Dale et al. (2001) Climate change and forest disturbancesa Biosciences181 Peterson (2003) Predicting the geography of species' invasions via

ecological niche modelingQuarterly Review of Biology

149 Schindler (2001) The cumulative effects of climate warming and otherhuman stresses on Canadian freshwaters in the newmillenniuma

Canadian Journal of Fisheries andAquatic Sciences

111 Magnuson et al. (1997) Potential effects of climate change on aquatic systems:Laurentian Great Lakes and Precambrian ShieldRegiona

Hydrological Processes

104 Mills et al. (2003) Lake Ontario: food web dynamics in a changingecosystem (1979–2000)

Canadian Journal of Fisheries andAquatic Sciences

102 Lavergne and Molofsky(2007)

Increased genetic variation and evolutionary potentialdrive the success of an invasive grass

Proceedings of the National Academyof Sciences

82 Clark et al. (2003) Estimating population spread: what can we forecast andhow well?a

Ecology

78 Starfield and Chapin(1996)

Model of transient changes in arctic and borealvegetation in response to climate and land use change

Ecological Applications

74 Kurz et al. (2008) Mountain pine beetle and forest carbon feedback toclimate changea

Nature

72 Hijmans and Graham(2006)

The ability of climate envelope models to predict theeffect of climate change on species distributionsa

Global Change Biology

aindicates climate change and IAS is a major focus of the article

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Several types of barriers were identified in the primary lit-erature review that hinder attempts to make IAS rangechange projections under climate change (Table 5). These in-cluded the failure of predictive models to integrate complex-ity (i.e., in the form of biotic interactions, and multiplecomponents of global change), variation in projections madeby different climate and niche models, and a lack of dataavailable to monitor the spread of IAS and to validate predic-tive models.Just over a third of the articles (34%) surveyed made rec-

ommendations to address the issue of climate change andIAS. The majority of these recommendations called for moreresearch on the subject (38%), followed by policy reform(23%), monitoring (20%), and scientific/technological advan-ces (15%). Recommendations for changes to societal behav-iour and education were rare (i.e., only 2% each of totalrecommendations). Recommendations were grouped into 17more detailed categories (Table 6).

DiscussionClimate change and IAS are among the top-five drivers of

biodiversity loss and changes to ecosystem services world-wide, along with habitat change, overexploitation of resour-ces, and pollution (MEA 2005). Individually, theseanthropogenic forces are causing significant changes to eco-systems and biota. In combination, the five drivers have syn-ergistic effects that are often complex, dramatic, and difficultto predict. Indeed, forecasting and planning for their interac-tions represents one of the greatest challenges for protectingbiodiversity in the future (Walther et al. 2009). Yet, tradition-ally, climate change and IAS are treated as separate problemsin policy and management, despite increasing evidence thatthe two are inextricably linked (Walther et al. 2009).Clearly, climate change will challenge our perception of

IAS. Some current IAS will diminish in impact, while otherswill intensify, and previously noninvasive taxa will becomeinvasive. Some native species will shift their geographic dis-tributions in response to changing environmental conditions

(Hellmann et al. 2008). Will we accept these species as suc-cessfully adapting to climate change or view them as pests?Invading species may also fill important ecological nichesleft empty by declining native species no longer adapted totheir local environments (Walther et al. 2009). Will we mod-ify our view of IAS if they play important roles in maintain-ing ecosystem function and services under climate change?Our consideration of what constitutes IAS will need to adaptin the face of climate change. Increasingly, we will be forcedto re-evaluate what we consider as ‘native’ versus ‘alien’, andas ‘migrations’ versus ‘invasions’.

Findings from the Knowledge SynthesisOur analysis of the primary literature suggests that the

topic of climate change affecting IAS range shifts is a rela-tively new area of research that garners little attention in thescholarly realm. While publications on climate change andIAS in general grew exponentially in the 1990s (Klenk etal.1), a focus on IAS range shifts under climate change is amore recent addition to the literature. According to our find-ings, only a handful of articles appeared on the topic prior to2001, and only in the past 3 years (2006–2009) has the num-ber of annual publications in the field actually begun to growconsistently, at least in a North American context.Despite the huge socio-economic implications of changing

IAS distributions under climate change, the topic is com-pletely absent from publications in the humanities, and iscovered infrequently in social science journals. Relativelyfew articles examine the topic from a multidisciplinary per-spective, combining ecological with social science considera-tions (e.g., McNeely 2001; Mainka and Howard 2010;Chornesky et al. 2005; Régnière et al. 2009; Roques 2010).Instead, most articles focus solely on the ecological dimen-sion of IAS under climate change, and appear in a widerange of natural science journals.The absence of a multidisciplinary approach to climate

change and IAS is surprising considering the extensive nega-tive impacts IAS can have, not only on native biodiversityand ecosystems, but also on the economy and other aspectsof society, such as resource industries and human health. Forexample, the cumulative cost of only 16 invasive species (outof a total of at least 1500) has been conservatively estimatedto be between $13.3 and $34.5 billion annually in Canada(Colautti et al. 2006). The current mountain pine beetle infes-tation has resulted in the loss of approximately 22% of Brit-ish Columbia’s merchantable lodgepole pine (Pinus contorta)since the 1990s, and is expected to lead to an 80% loss by2013 (Government of British Columbia 2006). Many of themost prevalent human diseases stem from IAS, includingsmallpox, HIV/AIDS, and cholera (Crowl et al. 2008).This state of affairs is inadequate given the complexity and

wide-ranging impacts of the climate change – IAS issue. In-deed, integrating knowledge and values across a range ofstakeholders and experts is increasingly becoming a commongoal of, and challenge in, forecasting, planning and policyevaluation processes in environmental management and con-servation. The failure to link ecological impacts of IAS rangechanges with subsequent impacts on human well-being is un-

Fig. 1. Cumulative number of articles published on climate changeand IAS.

1Klenk, N., Hewitt, N., and MacLellan, J.I. Unpublished. Invasive alien species and climate change: a bibliometric overview. Report preparedJune 2010, York University, Toronto, Ont.

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derscored by the lack of focus on economic and social sec-tors in the literature. Fewer than half of all studies we sur-veyed adopt a sectoral approach, and most of these examineforestry and fisheries considerations (e.g., Dale et al. 2001;Joyce et al. 2009; Prowse et al. 2009), while health and agri-culture are less commonly addressed (e.g., Waage and Mum-ford 2008; Hess et al. 2009).Many natural science journals have published articles on

the topic of climate change and IAS distributions over thepast 20 years, yet it is by no means a dominant topic, with amaximum of eight articles appearing in any particular journal.Several high-impact journals have featured articles on climatechange effects on IAS range change (e.g., Bohlen et al. 2004;Chornesky et al. 2005; Sharma et al. 2007; Hellmann et al.2008; Jackson et al. 2009), however, and several of the top-

cited articles from our analysis focus specifically on the issue,suggesting it is gradually gathering ‘scientific traction’, atleast within the natural sciences literature (Table 2).Our literature review revealed that most articles focus on

the potential shift of current IAS under climate change. Incontrast, anticipation of future biological invasions under cli-mate change is largely missing from the research (but seeMorrison et al. 2005; Cumming and Van Vuuren 2006; Sie-mann et al. 2007; Boonham et al. 2007; Pattison and Mack2008; Wirth et al. 2008; Diniz-Filho et al. 2009; Heino et al.2009; Bradley et al. 2010b). This gap may in part be due tothe inherent difficulties associated with predicting both futurebiological invaders (Ricciardi et al. 2011) and impacts of cli-mate change on individual biota (Bradley et al. 2010a; Vander Putten et al. 2010). Nonetheless, while a precise forecast

Table 3. Journals with three or more articles on climate change and IAS (Impact Factor is from 2010).

Journal title Impact Factor No. of articles Total articles (%)Global Change Biology 6.346 8 5Canadian Journal of Fisheries and Aquatic Sciences 2.166 6 4Journal of Biogeography 4.273 6 4Conservation Biology 4.666 5 3Biological Invasions 3.474 4 3Bioscience 5.510 4 3Frontiers in Ecology and the Environment 8.820 4 3Ambio 1.705 3 2Annals of the New York Academy of Sciences 2.847 3 2Canadian Journal of Plant Pathology 0.752 3 2Diversity and Distributions 4.248 3 2Forestry Chronicle 0.676 3 2Proceedings of the National Academy of Sciences 9.771 3 2

Table 4. Most frequently studied IAS in the primary literature review, all of which are currently present in Canada.

SpeciesNo. ofarticles

Actual or projected rangechange Impacts identified in the literature References

Lyme diseaseand deertick

6 Northward expansion predicted(up to 1000 km by 2080s)especially in eastern Canada

Emerging infectious disease in Canadawill disproportionately target vulnerablegroups (e.g., infants, elders, sociallyand economically marginalized)

Hess et al. (2009); Ogden et al.(2005); Ogden (2006); Ogdenet al. (2006); Ogden et al.(2008a); Ogden et al. (2008b)

Mountainpine beetle

5 Has already spread, continuedwarming will allow it toexpand further north, east andto higher elevations

Widespread tree mortality reducesforests’ ability to act as carbon sink

Carroll et al. (2004); Kurz et al.(2008); Logan and Powell(2004); Tkacz et al. (2008);Robertson et al. (2009)

Smallmouthbass

5 Northward expansion predicted Potential declines in native fish,particularly salmonids and cyprinids;over 25 000 populations of four nativecyprinids at risk

Jackson and Mandrak (2002);Sharma and Jackson (2008);Sharma et al. (2007); Sharmaet al. (2009a); Sharma et al.(2009b)

Gypsy moth 4 Northward expansion predicted Increased risk of invasion in Canadianforests, especially in west

Gray (2004); Logan et al.(2007); Tobin et al. (2007);Régnière et al. (2009)

Cheatgrass 3 Shift in range predicted leadingto both expansion andcontraction

Contraction could open up opportunitiesfor habitat restoration

Blumenthal et al. (2008); Brad-ley (2009); Bradley et al.(2009)

Kudzu 3 Increased atmospheric CO2anticipated to boost growingseason and facilitate spread atnorthern limit

Reduced native forest biodiversity,disruption of forest Ni cycles

Forseth and Innis (2004); Ziskaand George (2004); Bradleyet al. (2010b)

Zebra mussel 3 Expansion northward and tohigher elevations predicted

Ecological devastation of native speciesat all trophic levels

Thorp et al. (1998); Drake andBossenbroek (2004); Jilek etal. (2009)

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of invasion may be unrealistic, assessment of the relative riskof invasion by particular species is still possible. Predictivetools will increasingly be needed by managers and policymakers to prioritize invasion threats and effectively allocatescarce resources to areas most likely to be impacted by newIAS under climate change (Ricciardi 2003). In particular,comprehensive spatial bioclimatic modeling of IAS in Can-ada would enable rapid assessments of potential distributionsand impacts under climate change (McKenney et al. 2003;Kutz et al. 2004).Very little original research on climate change and IAS

range change within a Canadian context appears to exist inthe literature. Despite restricting our literature search to aCanadian focus, only a quarter of published papers we foundactually examined the issue from a Canadian perspective(e.g., Logan and Powell 2004; Mika et al. 2008; Sharma etal. 2009a; Landhausser et al. 2010). The majority of articlesgenerated in our search addressed the issue through surveysof existing literature, not through primary research. These lit-erature reviews considered climate-driven range shifts of IASas one of many topics covered under broader themes relatingto (i) climate change and IAS interactions (e.g., Jeschke andStrayer 2008; Dukes et al. 2009); (ii) IAS impacts (e.g.,McNeely 2001; Bohlen et al. 2004; Panov et al. 2007); and(iii) climate change impacts (e.g., Bradley et al. 2005; Parkin-son and Butler 2005; Scott and Lemieux 2005; Thuiller2007). Simulation/modeling studies were also fairly common,but field research was rare (i.e., only 11% of articles). Thismay reflect the predictive nature of the research, but ulti-mately the paucity of field observations or experiments mayjeopardize projections made in the lab, since field data arecritical for validating models (McKenney et al. 2003; Lee etal. 2008; Ogden et al. 2008a).There appears to be a bias in the literature toward studies

of terrestrial IAS, plants and invertebrates in particular. How-ever, this is consistent with the composition of currentlyknown IAS in Canada. According to the World ConservationUnion’s Global Invasive Species (GISP) Database, approxi-mately 115 IAS in Canada are terrestrial and approximately55 are aquatic (four species of amphibians and reptiles couldbe considered both terrestrial and aquatic; GISP 2010). Fur-ther, the majority of terrestrial species described in the data-base are plants (50%), followed by insects (17%). A wide

range of taxa are covered in our primary literature review, in-cluding all major taxonomic groups except reptiles and am-phibians (i.e., plants, invertebrates, fish, birds, mammals,microbes, fungi). Only 2% of the total known IAS in Canadaare reptiles or amphibians, which helps explain their absencefrom the literature. While the GISP numbers are undoubtedlyunderestimates of total IAS currently in Canada (e.g., Hen-drickson (2002) estimated that Canadian forests alone containat least 180 insect IAS feeding on woody plants), the propor-tions of different taxa coincide with those listed in Canada’sNational Invasive Alien Species Strategy (Government ofCanada 2004).No single species is a major focus of study on the effects

of climate change on distribution. The seven most frequentlystudied species appeared in only three to six papers on thistopic in our review. Three of these species, gypsy moth,kudzu, and zebra mussel, are listed among the top 100 worstIAS globally (i.e., considered to have serious negative im-pacts on biodiversity and (or) human activities; Lowe et al.2000). However, several other top 100 IAS that occur inCanada are addressed infrequently, if at all, within the litera-ture on IAS range shifts under climate change (e.g., fish hookflea (Cercopagis pengoi), is covered in one article: Panov etal. 2007; purple loosestrife (Lythrum salicaria); and Asianlonghorned beetle (Anoplophora glabripennis) are not cov-ered).All of the most frequently studied species from our review

have well-recognized impacts on humans (i.e., economic,health, or recreational consequences), which no doubt ac-counts for their relative prominence in the literature. All ofthese species are predicted to experience a northward expan-sion in their Canadian range under climate change. One spe-cies, the mountain pine beetle, has already spread north andeast of its native range in British Columbia, and to higher el-evations, as a result of climate change. The anticipated im-pacts of these IAS distribution changes in Canada will bewidespread. For example, the continued expansion of themountain pine beetle will negatively affect native biodiversityand ecosystem services through significant tree mortality andloss of forest carbon sinks (Kurz et al. 2008). Similarly, anorthward gypsy moth invasion in western Canada willthreaten forest health in that region (Régnière et al. 2009).The range expansion of smallmouth bass will have profound

Table 5. Barriers influencing the robustness of IAS range change projections.

Barrier ReferencesComplexity of interactions (e.g., biotic,global change)

Callaghan et al. (1995); Dale et al. (2001); Bradley et al. (2005); Keller (2007); Tombackand Resler (2007); Ruhl (2008); Bradley et al. (2010a); Roques (2010)

Precipitation projections (i.e., considerableuncertainty exists about future precipitationpatterns under climate change, climatechange models tend to exclude precipitationdata)

Callaghan et al. (1995); Siemann et al. (2007); Bradley (2009)

Variation in climate and niche models Logan et al. (2007); Lee et al. (2008); Diniz-Filho et al. (2009); Morin and Thuiller (2009)Lack of data (e.g., to monitor spread andvalidate models)

Peterson (2003); Forseth and Innis (2004); Tobin et al. (2007); Hellmann et al. (2008);Minns et al. (2008); Tkacz et al. (2008); Dukes et al. (2009); Heino et al. (2009)

IAS and climate change not consideredtogether and (or) stability assumed inclimate and species distributions

Scott and Lemieux (2005); Morin and Lechowicz (2008); Walther et al. (2009)

Unpredictability of future human actions(e.g., land use changes)

DeRivera et al. (2007); Hellmann et al. (2008); Dukes et al. (2009)

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consequences for native fish species, including the probableextirpation of at least four species in many Ontario lakes(Jackson and Mandrak 2002). The spread of Lyme diseaseup to 1000 km northward in eastern Canada is expected to

become a major public health issue over the next 70 years,as the disease will likely target vulnerable groups such as thevery young and very old, and those who are economicallymarginalized (Hess et al. 2009).

Table 6. Types of recommendations for addressing the interactive effects of climate change and IAS assembled from the primary literaturereview. Recommendation categories are ranked by the number of articles proposing such action.

Rank Recommendation categoryNo. ofarticles References Examples

1 Improve early detection andlong-term monitoringcapabilities

10 Boland et al. (2004); Kutz et al. (2004);Chornesky et al. (2005); Parkinson andButler (2005); DeRivera et al. (2007);Larson et al. (2007); Hess et al. (2009);Joyce et al. (2009); Prowse et al. (2009);Bradley et al. (2010b)

More diagnostic tools and personnel;proactive management

1 Improve modeling of IASunder climate change

10 Hijmans and Graham (2006); Thuiller(2007); Jeschke and Strayer (2008);Kurz et al. (2008); Lee et al. (2008);Dukes et al. (2009); Heino et al. (2009);Ogden et al. (2008a); Morin and Thuil-ler (2009); Tingley and Herman (2009)

Bioclimatic models for all North Ameri-can IAS; adoption of ecosystemapproach; inclusion of species interac-tions; use of field data to validatemodels; use of multiple modelingapproaches for robust predictions

2 Solve science–policydisconnect

6 Scott and Lemieux (2005); Ruhl (2008);Prowse et al. (2009); Lawler et al.(2010); Mainka and Howard (2010);Wiens and Bachelet (2010)

Explicitly address climate change andIAS interactions in conservation policyand planning

3 Integrate uncertainty intopolicy

4 Dukes et al. (2009); Evans and Perschel(2009); Lawler (2009); Lawler et al.(2010)

Allow for flexibility in policy andmanagement (adaptive management);recognize that ignorance, imprecision,stochasticity and surprises unavoidable

3 Increase research on theinteractive effects of climatechange and IAS

4 Marcogliese (2001); Scott et al. (2002);Keller (2007); Roques (2010)

3 Promote international coop-eration to address globalthreat of climate change andIAS

4 McNeely (2001); Callaghan et al. (2002);McKenney et al. (2003); Waage andMumford (2008)

4 Prepare for potential restora-tion opportunities whereIAS range contractionoccurs

2 Bradley et al. (2009); Bradley et al.(2010a)

4 Reduce agents of dispersal/create migration barriers

2 Bohlen et al. (2004); Rahel et al. (2008) Through education, trade changes, limitsto development

5 Study effects of rising CO2 onIAS plants

1 Ziska and George (2004)

5 Reduce greenhouse gases toprevent future IAS

1 Hess et al. (2009)

5 Anticipate increased burdenon medical system

1 Hess et al. 2009

5 Build ecosystem resilience toinvasions

1 Waage and Mumford (2008)

5 Encourage cooperation betweenclimate change scientistsand invasion ecologists

1 Higgins et al. (2003)

5 Conduct regional scaleresearch of effects ofclimate change on IAS

1 Hongoh et al. (2009)

5 Increase baseline knowledgeof IAS ecology

1 Kutz et al. (2004)

5 Investigate global effects ofgardening and urbanlandscaping

1 Niinemets and Penuelas (2008)

5 Adopt a flexible perspectiveon IAS under climatechange

1 Walther et al. (2009) ‘Invading’ species may enrich localbiodiversity impoverished by climatechange

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Many papers discussed uncertainties and assumptions thatact as obstacles to the reliable prediction of biological inva-sions under climate change. One significant area of uncer-tainty relates to the integration of complex ecological andenvironmental data into predictive models. IAS have complexinteractions with both the native biological communities theyinvade and with climate change, and these relationships andresulting impacts can be difficult to forecast (Dale et al.2001; Bradley et al. 2005). In some cases, biotic and abioticinteractions can have unexpected outcomes, as has beenfound with the invasive fungus whitebark pine blister rust(Cronartium ribicola) in alpine treeline habitats. Changes tothe treeline have been proposed as a bioindicator of climatechange, but the increased incidence of fungal rust under cli-mate change may actually delay or inhibit treeline responseto climate warming (Tomback and Resler 2007). Conse-quently, predictive models of treeline change need to accountfor the confounding effects of IAS pathogens on distributionpatterns. Possible positive feedback loops between climatechange and IAS also need to be anticipated. For instance, cli-mate change is promoting the spread of mountain pine beetleto the north and east of its native range in western Canada.The resulting widespread tree mortality caused by the beetleinfestation is threatening forests’ ability to act as carbonsinks, instead turning decaying forests into carbon sources(Kurz et al. 2008).Another area of uncertainty is the variability inherent to

climate and species distribution models. Not only is it chal-lenging to integrate data with different temporal and spatialscales, but alternative types of models (e.g., niche-based ver-sus process-based distribution models and different climatechange scenarios) can produce divergent predictions (Lee etal. 2008; Diniz-Filho et al. 2009). To increase the accuracyof predictive models, authors thus recommend adoptingstandardized methods to measure biotic requirements, andthe comparison of multiple model types (Lee et al. 2008;Morin and Thuiller 2009).A further impediment to the development of robust predic-

tions on species range shifts under climate change is the lackof ecological data on IAS and the habitats they invade. Base-line information on the state of different ecosystems is largelyunavailable because of an absence of large-scale and long-term monitoring programs. Canada does not have a nationalnetwork of forest health plots, for example, which makes itdifficult to effectively assess the impacts of invasive forest in-sects and pathogens (Tkacz et al. 2008). Although the borealforest region is expected to be particularly vulnerable to bio-logical invasions of southern species under climate change,no studies have yet examined the interactions of climatechange and IAS on freshwater biodiversity in this ecoregion(Heino et al. 2009). Similarly, our ability to forecast futureimpacts of the highly invasive kudzu vine (which recentlyspread north into Canada) is severely limited because littleresearch has been conducted on the ecological effects of thespecies (Forseth and Innis 2004). We lack basic informationon the spread of most IAS in North America. However, theaccurate tracking of IAS movements can be relatively simple,and need not require a sophisticated and time-intensive mon-itoring protocol (Tobin et al. 2007).Perhaps the most serious barrier to effective IAS range

change projections comes from our failure to fully acknowl-

edge the dynamic and interactive nature of climate changeand IAS. This exemplifies a larger problem related to ourlimited understanding of the interactions of multiple stressorsin general and their impacts on species and ecosystems(Fleishman et al. 2011). Despite the complex and significantinteractive effects of climate change and IAS on global biodi-versity, the two drivers of global change continue to be con-sidered in isolation in policy and management (Walther et al.2009). Additionally, policy is based on outdated assumptionsof biogeographic and climatic stability. For example, a pro-tected areas policy in Canada supports the ongoing protectionof existing ecological communities but does not account forthe changing distribution or ecological integrity of thesecommunities under climate change (Scott and Lemieux2005).A wide range of recommendations for addressing the inter-

active effects of climate change and IAS were made in theprimary literature. Most recommendations referred to theneed for more research, policy and management reform ormonitoring of trends. There was a general consensus amongstudies that the current lack of quantitative data severely im-pedes our ability to make accurate predictions of futuretrends and impacts, and consequently to formulate effectiveresponses to the problem. For example, Dukes et al. (2009)recommended that more bioclimatic modeling be undertakento predict the potential ranges of IAS in northeastern NorthAmerican forests under climate change, complimented withresearch into how demographic processes and competitionmight influence their shifting distributions. Hijmans and Gra-ham (2006) stressed the need to validate such bioclimaticmodels, through improved knowledge of current distribu-tions, and integration with information on species’ physiol-ogy. Ziska and George (2004) called for additional studies todetermine how IAS plants respond to rising CO2 levels, sothat adaptation, mitigation, and management strategies couldbe developed. Similarly, Prowse et al. (2009) suggested thatthe development of integrated field-based monitoring and re-search programs, together with predictive models, would al-low significant uncertainties to be addressed in our ability toforecast climate change impacts in northern Canada.Interestingly, very few papers called for more education or

changes to societal behaviour (e.g., educating anglers aboutearthworm introductions, Bohlen et al. 2004; discouragingthe use of IAS plants by the horticultural industry, Larson etal. 2007). This may partially reflect the fact that most papersappeared in natural science journals and consequently werenot focused on social dimensions of the issue.Additionally, because the scholarly literature on climate

change – IAS interactions is in its infancy, recommendationsmay be weighted more toward generating knowledge and de-veloping policy on the topic, rather than on disseminating in-formation to the public, which might come at a later stage.However, while a focus on the interactive effects of climatechange and IAS may be new, this research draws on thebroader ecological and climate change literature, perhaps ac-counting for the high number of literature reviews. The mostcommon recommendations were to improve early detectionand monitoring capabilities (e.g., through the development ofdiagnostic tools and assignment of dedicated personnel; Bo-land et al. 2004; de Rivera et al. 2007; Joyce et al. 2009)and to improve modeling of IAS under climate change (e.g.,

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by developing bioclimatic models for all North AmericanIAS, by integrating a variety of abiotic and biotic data intomodels, and by validating with field data; Thuiller 2007;Kurz et al. 2008; Dukes et al. 2009). The need to explicitlyaddress climate change – IAS interactions in research andpolicy (e.g., Scott et al. 2002; Keller 2007), and to embraceuncertainty through adaptive management (e.g., Evans andPerschel 2009; Lawler et al. 2010) were also key recommen-dations in the literature.

Bridging the science–policy gapThe mobilization of knowledge from scholarly research

into policy is a notorious challenge for scientists (Norton1998; Likens 2010; Osmond et al. 2010; Pace et al. 2010).Scientific and technological information can provide impor-tant insight and perspective on environmental issues neces-sary for effective policy-making. However, numerous culturaland procedural barriers exist along the path from knowledgegeneration to decision-making that impede engagement ofscientists in the policy process (Pouyat et al. 2010). Amongthese are the difficulties associated with gaining exposure forresearch beyond the academic realm, communicating scien-tific information to a wider audience, and navigating throughdiverse and often conflicting opinions and agendas on envi-ronmental issues (Likens 2010). As a result, a significant de-lay typically exists between the discovery and investigation ofan environmental problem and public and political responsesto the issue. Indeed, the actual formulation and implementa-tion of policy and management on environmental problemscan take years or even decades, even if research suggests ur-gent action is required (Meyer et al. 2010; Pouyat et al.2010).The newness of the field, the complexity of the interac-

tions between climate change and IAS, and the uncertaintiesinvolved in predicting IAS range changes under climatechange no doubt explain, in part, why policy is lacking onthis issue at both federal and provincial/territorial levels inCanada. Nonetheless, there is a growing awareness of thecomplexity (Roe 1998), or ‘wickedness’ (Rittel and Webber1973), and (or) ‘post normal’ (Funtowicz and Ravetz 1993)nature of many of the environmental problems facing deci-sion-makers today, such as climate change and IAS. Ritteland Webber (1973) argued that these types of problems areexceptionally difficult to resolve because they are particularlyvulnerable to framing conditions (i.e., how they are presentedaffects perception and response), affect numerous stakehold-ers, are plagued by large uncertainties, involve often incom-patible criteria for judging the ‘goodness’ of decisions, andoffer no enumerable or exhaustive set of possible solutions.Consequently, the science that informs policy developmentin addressing these ‘wicked’ problems requires disciplinary,multidisciplinary, and transdisciplinary approaches.

ConclusionOur knowledge synthesis revealed that research on IAS

range shifts under climate change is in its infancy in Canada,although it appears to be a growing field of study. While ourunderstanding of the impacts of climate change on IAS distri-butions in Canada is incomplete, scientific information is ac-cumulating with which policy can be informed and directed.For example, research predicts the emergence of numerous

new infectious diseases in arctic Canada with rising temper-atures, highlighting the need for coordinated circumpolar dis-ease monitoring, and extensive health care planning to handlethis new pressure. Improved and more extensive bioclimaticmodeling will be essential for mounting an effective policyresponse to IAS range shifts under climate change across thecountry. These models can be used to anticipate where pestsmight spread in the future, so that early detection and rapidresponse efforts are targeted to specific geographic regions,and scarce IAS management resources are used efficiently.The multidisciplinary dimensions of the climate change –

IAS issue are largely overlooked in the scholarly literature,with most studies having a purely ecological perspective. Fur-thermore, research focuses on modeling range changes ofcurrent IAS threats, rather than predicting potential futureIAS threats. Authors working in the field identify many bar-riers to the development and implementation of robust pre-dictive tools on IAS range shifts under climate change. Inparticular, continual support for the paradigm of a static cli-mate and static species distributions in the research commun-ity is seen as a major problem. Additionally, unless there is aconcerted effort by decision-makers to consider the dynamicinteractive nature of climate change and IAS, the ability todevelop effective policy clearly will be undermined.

AcknowledgementsThis knowledge synthesis was funded by the Canadian

Foundation for Climate and Atmospheric Sciences. AnnetteDubreuil provided project management. We are grateful forthe comments of two anonymous reviewers on an earlier ver-sion of this paper.

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