Diversity and Distributions, (Diversity Distrib.) (2009) 15, 831–840

BIODIVERSITY RESEARCH

Predicting introduction, establishment and potential impacts of smallmouth bass Sapna Sharma1*, Leif-Matthias Herborg2,3 and Thomas W. Therriault2

1

Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3G5, 2Pacific Biological Station, Fisheries and Oceans Canada, Nanaimo, BC, Canada V9T 697, 3Fisheries Science Section, Ministry of Environment BC, Vic., Canada V8W 9M1

ABSTRACT Aim The introduction of non-indigenous species has resulted in wide-ranging

ecological and economic impacts. Predictive modelling of the introduction and establishment of non-indigenous species is imperative to identify areas at high risk of invasion to effectively manage non-indigenous species and conserve native populations. Smallmouth bass (Micropterus dolomieu), a warm water fish species native to central North America has negatively impacted native fish communities, including cyprinids and salmonid populations, as a result of intentional introductions. We predicted the introduction risk; species establishment based on habitat suitability; identified lakes at high risk of invasion; and finally assessed the consequential impacts on native salmon, trout and cyprinid populations. Location Ontario and British Columbia, Canada. Methods Classification tree and logistic regression models were developed and validated to predict the introduction and establishment of smallmouth bass for thousands of lakes. Results Densely human populated areas and larger lake surface areas successfully identify lakes associated with the introduction of smallmouth bass (introduction model) in British Columbia. Climate, lake morphology and water chemistry variables were the driving environmental parameters to define suitable smallmouth bass habitat (establishment model). A combination of the introduction and establishment model identified 138 lakes that are currently at risk in British Columbia to the introduction and establishment of smallmouth bass. Of these 138 high-risk lakes, 95% of them contain at least one species of salmon, trout or cyprinid, thereby increasing the potential impact of an invasion by smallmouth bass. Main conclusions Our framework can be applied to other terrestrial and aquatic species to obtain a better understanding of the potential risk posed by a nonindigenous species to an ecosystem. Furthermore, our methodology can be used to focus management efforts on areas at higher risk (e.g. number of potential releases, more favourable habitats) to control future introductions of nonindigenous species, thereby conserving native populations.

*Correspondence: Sapna Sharma, De´partement de Sciences Biologiques, Universite´ de Montre´al, Montreal, QC, Canada H3C 3J7. E-mail: [email protected]

Keywords Biological invasions, classification tree, cyprinids, invasive species, logistic regression, salmonids.

Spread of non-indigenous species is a major cause of global biodiversity loss in a wide range of habitats including

freshwater ecosystems (Sala et al., 2000). In North America, freshwater biodiversity is under threat from numerous nonindigenous species with well-documented ecological and economic impacts such as the zebra mussel (Ricciardi &

ª 2009 Blackwell Publishing Ltd

DOI: 10.1111/j.1472-4642.2009.00585.x www.blackwellpublishing.com/ddi

INTRODUCTION

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S. Sharma et al. MacIsaac, 2000; Pimentel et al., 2005). Because of the range and severity of environmental and socioeconomic impacts reported for aquatic invasive species (AIS), the ability to predict their potential distribution is critical for their control and management. The distribution of AIS is determined by the four steps of the invasion process: arrival, survival, establishment and spread. Initial arrival is due to human-mediated introduction via one or more vectors. Once introduced, survival and establishment are dependent on the organism’s ability to adapt, survive and reproduce in this new environment (Guisan & Thuiller, 2005). If the species becomes established (e.g. self-sustaining population), secondary spread can either occur through human-mediated transport or natural dispersal (Colautti & MacIsaac, 2004). Combining predictions of introduction and establishment, the potential distribution of an AIS can be predicted (Herborg et al., 2007a). Here we develop models for introduction, establishment and impact using a global freshwater invader with welldocumented habitat preferences and impacts on native fishes, smallmouth bass (Micropterus dolomieu), as an example. Smallmouth bass is a warm water fish species native to central and eastern North America (Scott & Crossman, 1998). Since the mid-1800s, the range of smallmouth bass has expanded both across North America and throughout Europe, Russia, Asia and Africa as a result of intentional introductions to provide angling opportunities (Scott & Crossman, 1998). In its invaded range in western North America, smallmouth bass primarily impact salmon fry and smolts via predation (Harvey & Kareiva, 2005). Removal of smallmouth bass from a Columbia River reservoir increased the production of chinook salmon (Oncorhynchus tshawytscha) and steelhead (Oncorhynchus mykiss) (Harvey & Kareiva, 2005), confirming the negative impacts of this invader. Furthermore, the presence of smallmouth bass has been shown to reduce growth, survival and fecundity of lake trout (Salvelinus namaycush) as smallmouth bass out-compete this species for forage fish (Vander Zanden et al., 1999) and can lead to the homogenization of fish fauna as cyprinid species are lost (MacRae & Jackson, 2001; Jackson, 2002). The purpose of this study was to predict the introduction, establishment and implications of smallmouth bass invasions in British Columbia. We achieved this purpose via four objectives: (1) prediction of the most likely locations for introduction of smallmouth bass in British Columbia; (2) development of species occurrence models to predict establishment for smallmouth bass using environmental variables – these models were developed for Ontario lakes where smallmouth bass have established populations and validated for a subset of lakes in Ontario and all known populations in British Columbia; (3) identification of regions in British Columbia that are at high risk for the introduction and establishment of smallmouth bass based on the combination of introduction and establishment models; and (4) assessment of the prevalence of native salmon, trout and cyprinid species in British Columbia lakes predicted to be at high risk of invasion from smallmouth bass.

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METHODS Data acquisition Species introduction model We based our introduction model on four variables: lake size (ha), lake perimeter (m), distance to the nearest road (km) and the human population in the area. These variables were selected based on the existing literature predicting the risk of human-mediated introductions to freshwater lakes (Bossenbroek et al., 2001; MacIsaac et al., 2004; Muirhead & MacIsaac, 2005). A digital map of lakes in British Columbia specifying lake location and shape was obtained from the British Columbia Ministry of Environment and included 67,463 lakes in British Columbia. Lake surface area and perimeter were calculated for each lake using Hawth’s tool (available at http://www.spatialecology.com) within ArcGIS 9.1. Census data for 1996 were obtained from Natural Resources Canada (http://www.geogratis.gc.ca/geogratis/en/collection/search.do) and overlaid with each lake using the Spatial Analyst extension within ArcGIS 9.1. The shortest distance from any paved road or major unpaved road to each lake in British Columbia was calculated with the same tool. Presence and absence datasets for smallmouth bass were constructed by including species occurrence data (64 lakes) and by generating one-hundred randomly selected lakes as absence data. Each dataset was randomly divided based on an 80 : 20 ratio to provide training and validation datasets. That is, 80% of the data were retained to construct the models and 20% of the data were used to evaluate the models independently. Species establishment model We obtained data for smallmouth bass occurrence from the Ontario Habitat Inventory Index, which summarizes species occurrence, geographical location, physical habitat and water chemistry for Ontario lakes. There were 1485 occurrences and 6082 recorded absences of smallmouth bass in the dataset. The Ontario dataset was randomly divided into training and validation datasets with the same large-scale geographical coverage in both datasets based on an 80 : 20 ratio. We obtained data for smallmouth bass presence data for 1885 lakes in British Columbia from the British Columbia Ministry of Environment. Mean monthly air temperature data were obtained from the WorldClim database (http:// www.worldclim.org) and provided on a 30 arc seconds1 km resolution. Nineteen environmental predictor variables were used for the species establishment model: lake perimeter (m), lake surface area (ha), maximum depth (m), elevation (m), surface pH, surface total dissolved solids concentration (mg L)1), Secchi depth (m) and mean monthly air temperatures (C). Physical habitat and water chemistry variables were attained from the Ontario Habitat Inventory Index and British Columbia Ministry of Environment.

Diversity and Distributions, 15, 831–840, ª 2009 Blackwell Publishing Ltd

Predicting the invasion of smallmouth bass Model development We used the statistical approaches in our study that best reflected the structural properties of the datasets and provided the highest predictive power when validated on independent datasets. Species introduction model Classification trees predicted species occurrence based on lake morphology, road distance and human population census data in British Columbia. Classification trees were run in sas, based on the chi-squared distance and were significant at a < 0.05. The algorithm that was used minimizes misclassification rates when dividing the data at each split. We used a cross-validation approach and calculated the number of leaves required to minimize the proportion of misclassifications to identify the maximum depth of the classification trees. Classification trees are generated by continually dividing the data into two groups with the division based on the predictor that best divides the group of observations such that they are as mutually exclusive and homogenous as possible (De’ath & Fabricius, 2000; Olden & Jackson, 2002; Sharma & Jackson, 2008). The classification trees were evaluated on independent, validation datasets to calculate overall classification rate (correctly predicting species presence and absence), sensitivity (correctly predicting species presence) and specificity (correctly predicting species absence). Following evaluation, the models were extrapolated to British Columbia to identify regions in which smallmouth bass could be successfully introduced.

Instead of designating species presence by the traditional decision threshold of 0.50, we constructed Receiver Operating Characteristic (ROC) curves (Fielding & Bell, 1997; Olden & Jackson, 2002). ROC curves are particularly useful with datasets that have unequal species presence and absence data as logistic regression tends to produce scores that are biased towards the more prevalent group (Fielding & Bell, 1997). The ROC analyses were used to identify species thresholds, which would minimize false absences, thereby increasing the measure of sensitivity as this study is modelling non-native species and their introduction and establishment (i.e. minimizing Type II error). Based on the ROC analyses and the optimal decision threshold, we constructed ‘confusion matrices’ using the independent, Ontario validation dataset (Fielding & Bell, 1997). The confusion matrix summarizes true absence, true presence, false absence and false presence, which can then be used to calculate overall classification rate, sensitivity and specificity (Fielding & Bell, 1997; Olden & Jackson, 2002). Introduction and establishment model We identified British Columbia lakes with a potential for smallmouth bass introduction and establishment by combining the species introduction model and establishment model. We overlaid the geographical layer of lakes with a potential for species introductions with the geographical layer of lakes with predicted suitable habitat in ArcGIS 9.1. Subsequently, we compared the lakes predicted by this combined model with British Columbia lakes actually invaded by smallmouth bass for validation.

Species establishment model

Impacts on native species

Multicollinearity between variables was evaluated using bivariate plots and correlation analyses prior to regression analyses to determine which variables should be retained. In addition, variables were log transformed as necessary to satisfy assumptions of normality. Variables included in the models were surface area, maximum depth, perimeter, elevation, secchi depth, pH, total dissolved solids concentration and mean monthly air temperatures. Stepwise multiple logistic regression models were constructed for Ontario lakes using the training dataset in sas to evaluate the relationship between smallmouth bass occurrence and physical habitat, water chemistry and climatic predictor variables. In a logistic regression, response variables are subject to a logit transformation, whereas predictor variables are based on a linear combination using maximum likelihood (Olden & Jackson, 2002; Sharma & Jackson, 2008). Significance values were set at a value of a = 0.05 for predictor variables to enter and remain in the model. Logistic regression models were tested on the independent Ontario validation dataset and the British Columbia presence dataset. Following validation, we applied the logistic regression models to all lakes in British Columbia to identify the potential occurrence of smallmouth bass based on habitat suitability.

Following identification of lakes at high risk of invasion by smallmouth bass, we identified the number of salmon populations: chinook salmon (Oncorhynchus tshawytscha), chum salmon (Oncorhynchus keta), coho salmon (Oncorhynchus kisutch), pink salmon (Oncorhynchus gorbuscha) and sockeye salmon (Oncorhynchus nerka); trout populations: bull trout (Salvelinus confluentus), cutthroat trout (Oncorhynchus clarki), dolly varden (Salvelinus malma), lake trout (Salvelinus namaycush) and steelhead (O. mykiss); and cyprinid populations: lake chub (Couesius plumbeus), peamouth chub (Mylocheilus caurinus) and redside shiner (Richardsonius balteatus). The quantification of species occurrence that may be negatively impacted by the introduction of smallmouth bass provides an estimate of the potential impacts of smallmouth bass invasions on native fish populations and is useful for increasing the impact score for more ‘sensitive’ species. RESULTS Species introduction model Human population size and lake surface area were the most important predictors of smallmouth bass occurrence in British

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S. Sharma et al. evaluated on the independent, validation dataset was c. 84.5 %, with 90.2% sensitivity and 61.3% specificity for smallmouth bass. Applying the predictive models to the independent British Columbia species occurrence dataset, 75.7% (28 of 37) of species presence was correctly predicted. Extrapolation of the models to lakes in British Columbia revealed suitable habitat for the occurrence of smallmouth bass in 1052 lakes in most central and southern watersheds in British Columbia and unsuitable habitat for the occurrence of smallmouth bass in northern British Columbia watersheds (Fig. 3). Introduction and establishment model Figure 1 Summary of classification tree analysis predicting smallmouth bass occurrence in British Columbia based on lake morphology, distance to road and human population census data.

Columbia based on the classification tree analysis (Fig. 1). Evaluation of the independent validation dataset showed that overall classification success was 93.5%, with 83.1% sensitivity and 100% specificity. Extrapolation of the classification tree model for British Columbia identified 727 lakes, concentrated on Vancouver Island, the lower Fraser, and the Thompson and Columbia watersheds that were at high risk of smallmouth bass introduction (Fig. 2). Species establishment model Climatic, physical habitat and water chemistry variables were important predictors of smallmouth bass occurrence based on stepwise multiple logistic regression analyses (see Appendix S1 in Supporting Information). Overall classification success as

We identified 138 lakes that are currently suitable for the introduction and establishment of smallmouth bass (Fig. 4, Appendix S2) in British Columbia. The combined introduction and establishment model correctly predicted smallmouth bass occurrence in 26 of 37 (70.3%) British Columbia lakes suggesting these lakes are at high risk of invasion. Furthermore, there are a high number of vulnerable lakes on Vancouver Island, with another cluster in the lower Fraser River drainage, and some lakes in the upper Fraser, the Thompson and Columbia River drainages. Impacts on native fishes There are 138 lakes that are currently suitable for the introduction and establishment of smallmouth bass in British Columbia. Twenty of the 138 high risk lakes (14.1%) contain at least one salmon species, while 122 of the 138 lakes (88.4%) contain at least one species of trout and 29 lakes (21.0%) contain at least one cyprinid species (Table 1, Appendix S2).

Figure 2 Predicted introduction of smallmouth bass in British Columbia based on the species introduction model. Watersheds are highlighted for the Fraser, the Thompson and the Columbia.

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Predicting the invasion of smallmouth bass

Figure 3 Predicted habitat suitability of smallmouth bass in British Columbia based on the species establishment model. Watersheds are highlighted for the Fraser, the Thompson and the Columbia.

Figure 4 Predicted introduction and establishment of smallmouth bass in British Columbia. Watersheds are highlighted for the Fraser, the Thompson and the Columbia.

DISCUSSION There is a growing demand for tools that can support, defensible, knowledge-based decision making for those managing invasive species (Lodge & Shrader-Frechette, 2003; Simberloff et al., 2005). For example, tools that allow one to predict the potential distribution for a non-native species,

including its likelihood of arrival and establishment, inform risk assessments and help decision makers prioritize limited resources for control and management. A wide variety of predictive models have been applied to non-native species but most have focused on only single steps in the invasion cycle. For example, some studies focused on a particular introduction pathway such as ballast water (Wonham et al., 2005;

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S. Sharma et al.

Salmon species

Trout species

Cyprinids

No. species present

No. lakes

Percentage of lakes

No. lakes

Percentage of lakes

No. lakes

Percentage of lakes

0 1 2 3 4 5

118 12 3 2 – 3

85.5 8.7 2.2 1.4 – 2.2

16 75 31 15 1 –

11.6 54.3 22.5 10.9 0.7 –

109 20 8 1 – –

79.0 14.5 5.8 0.7 – –

Drake & Lodge, 2007) or trailering boats between freshwater lakes (Johnson et al., 2001). Others have attempted to predict the likelihood of establishment for a particular species. For example, in freshwater systems, environmental niche modelling has been used to successfully identify suitable areas for establishment at larger spatial scales (Drake & Bossenbroek, 2004; Herborg et al., 2007b) but lack individual lake predictions. Vander Zanden et al. (2004) developed a more comprehensive approach for Ontario lakes by developing environmental suitability models for smallmouth bass using artificial neural networks and identified a number of vulnerable lake trout populations using stable isotope analyses. The specificity of this approach requires intensive data not often available for new introductions. Our study is one of the first to fill this void. Although complimentary as we also developed environmental suitability models with high predictive power for smallmouth bass, our approach allowed the prediction of suitable habitat for smallmouth bass in British Columbia using a less data-intense approach and relatively few occurrences of smallmouth bass in British Columbia compared with Ontario. In addition, we developed a species introduction model identifying the vectors of smallmouth bass invasion and compared the potential bass distribution with current occurrences of salmon, trout and cyprinid populations to characterize the potential impacts of smallmouth bass introductions in British Columbia. Furthermore, we present a comprehensive case study to decrease the likelihood of smallmouth bass invasions in British Columbia as suggested by the framework proposed by Vander Zanden & Olden (2008). Species introduction model As the most likely pathway for the introduction of smallmouth bass into previously uninvaded watersheds in British Columbia is through intentional illegal introductions by anglers to establish a recreational fishery, the prediction of future invasions is particularly difficult. These intentional introductions represent rare, non-random events, unlike other case studies of freshwater introductions where unintentional introductions were modelled. A widely used approach for predicting accidental introductions of non-native freshwater species like zebra mussels and spiny water flea are gravity models (Leung et al., 2006; Muirhead et al., 2006). While this method has very successfully modelled invasion progress, it is very data intense

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Table 1 Lakes identified at risk to the introduction and establishment of smallmouth bass in British Columbia. The number and percentage of lakes predicted at risk are summarized by the number of salmon, trout species and cyprinids found in each lake. For a complete listing of all lakes, see Appendix S1.

and based on the assumption that lake attractiveness (often related to lake size) and distance to infested lakes determine the likelihood of becoming invaded, which may or may not be true for intentional introductions. In addition, there are no province-wide creel surveys or more detailed angler information available to permit such an analysis for British Columbia. Our predictions determined that the primary factors associated with potential introductions into lakes are human population size in the district the lake is located in and surface area of the lake. This agrees with findings by Reed-Andersen et al. (2000), who found a strong correlation between the area of lakes in Wisconsin and the number of recreational boats using them. Similarly, the introduction risk of zebra mussels into inland lakes through human-mediated transport has been reported to increase with lake size (Kraft & Johnson, 2000). The classification tree models were successful at predicting lakes with introduced smallmouth bass, and future surveys of angler behaviour and movements could provide data for more advanced predictions. Future introduction hotspots are highlighted in our predictions. These areas should be the focus of future management and public awareness efforts to minimize the probability of future introductions. Predictions generated by the species introduction model may be impacted by changing human population size and this may influence our understanding of biological invasions. Smallmouth bass may be introduced in locations with relatively low human densities by fishing interests in an effort to increase income at relatively remote locations or by anglers who would rather not drive long distances to catch smallmouth bass. As anthropogenic interference increases, species introduction models may be improved by acknowledging and accounting for the possibility that parameters accounting for the ‘reach of human influence’ may be more appropriate than traditional human census data. Species establishment model Climatic, physical habitat and water chemistry information were important predictors of smallmouth bass occurrence. We developed models for Ontario, a province where smallmouth bass are well established, to predict establishment in British Columbia. We found that 38.6% of lakes currently contain suitable environmental conditions for smallmouth bass to establish. Smallmouth bass occurrence was related to fall air temperatures, lake surface area and maximum depth.

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Predicting the invasion of smallmouth bass Smallmouth bass tend to be found in larger and deeper lakes and rivers (Scott & Crossman, 1998). The positive relationship between lake size and smallmouth bass occurrence may be partially explained by the tendency to sample larger and more accessible lakes (Minns, 1986). Air temperature has been found to be a strong predictor of smallmouth bass distribution (Shuter et al., 1980; Dunlop & Shuter, 2006) as smallmouth bass growth (Shuter et al., 1980; Casselman et al., 2002; Shuter & Ridgway, 2002) and year-class strength (Casselman et al., 2002) have been related to summer air temperatures. The establishment of a successful smallmouth bass population is dependent partly on the ability of young-of-the-year smallmouth bass to survive the winter as larger young are able to survive starvation and winter conditions better than smaller fish (Shuter et al., 1980; Wismer et al., 1985). In years with increased fall temperatures, growth of young smallmouth bass may be enhanced, thereby increasing overwintering survival of young-of-the-year fish. Introduction and establishment model The combination of the introduction and establishment model allows the prediction of the two initial steps of the invasion cycle: introduction and establishment. While the number of invaded lakes for validation is limited by data availability, most lakes with smallmouth bass were correctly predicted in the combined model. Lakes with species absence in British Columbia were not included in the model validation, as those lakes may or may not become invaded in the future. There are very few studies that have attempted to include both steps of the invasion process into predictions of overall risk. The occurrence of invasive plants has been predicted on the combination of classification tree based environmental models and measures of propagule pressure (Rouget & Richardson, 2003). Contrary to our study, this approach included natural dispersal as a measure of propagule pressure, rather than human-mediated transport. Leung & Mandrak (2007) combined a neural network-based environmental model with a gravity model predicting angler movements to identify lakes at threat from zebra mussel invasions. Their predictions were based on a well-studied invader with high data resolution for vector traffic, allowing them to include time-dependent introduction risk. Vander Zanden et al. (2004) used road access data in artificial neural networks to predict smallmouth bass occurrence and food web interactions to predict their impact on lake trout populations in Ontario lakes. The combined introduction and establishment model presented in our study predicted several watersheds that are at greater risk from future invasions of smallmouth bass. One potential hotspot is a cluster of lakes on central Vancouver Island. Two other clusters predicted for smallmouth bass introductions are in the upper Fraser River and in the Thompson River (a tributary to the Fraser River). In addition, in the Columbia basin, a number of lakes are predicted to be at risk from introductions. The Fraser River and its tributaries, as well as

watersheds in Central Vancouver Island, support numerous salmon stocks, which could be at further peril if smallmouth bass become established in these lakes. Implications The widespread introduction and potential spread of top predators, including smallmouth bass, are likely to have negative implications for native fish populations in British Columbia watersheds. For example, smallmouth bass could have a serious impact on the productivity and viability of salmon populations, especially because a significant number of lakes (14.1%) at risk of potential invasion by our introduction and establishment model also support salmon. Smallmouth bass are known to predate upon salmon fry and smolts (Fritts & Pearsons, 2004, 2006; Harvey & Kareiva, 2005). Migrating salmon species are particularly vulnerable to predation by smallmouth bass if habitat is shared during salmon runs. Tabor & Wurtsbaugh (1991) showed that predation on chinook salmon is high during the spring and early summer when the habitat of abundant fry and sub-yearling chinook salmon overlaps with smallmouth bass. Bennett et al. (1991) found that migrating juvenile salmon were the dominant forage fish species for smallmouth bass in the Columbia River in the spring. The introduction of littoral predators, such as smallmouth bass, may have negative implications for trout populations. In our analyses, 88.4% of lakes predicted to be at risk for introduction and establishment of smallmouth bass contained native trout species. The introduction of smallmouth bass may decrease the growth, survival and fecundity of native top predators such as lake trout populations via shared food resources in the absence of pelagic forage fish species (Vander Zanden et al., 1999, 2004). Sharma et al. (in press) estimated that c. 20,000 Canadian lake trout populations could be threatened because of the northward range expansion of smallmouth bass and climate change. In addition, the introduction of smallmouth bass to lakes with brook trout has resulted in decreased abundance of brook trout, which has been attributed to out-competition by smallmouth bass for shared forage species and predation by smallmouth bass on young-of-the-year brook trout in spring (Olver et al., 1991). Many studies have reported that the presence of littoral predators has been associated with the absence of cyprinids (e.g. Harvey, 1981; Tonn & Magnuson, 1982; Findlay et al., 2000; MacRae & Jackson, 2001; Vander Zanden et al., 2004). Cyprinids were present in 21% of the lakes predicted to be at risk by our introduction and establishment model. Introduction of littoral predators like smallmouth bass into an aquatic system may result in the loss of entire assemblages leading to homogenization of fish fauna (Rahel, 2000, 2007; Jackson, 2002). Jackson & Mandrak (2002) estimated that more than 25,000 local populations of four cyprinid species, specifically northern redbelly dace (Phoxinus eos), finescale dace (Phoxinus neogaeus), fathead minnow (Pimephales promelas) and pearl dace (Margariscus margarita), may disappear within Ontario

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S. Sharma et al. alone as smallmouth bass expand their invaded range as a result of climate change. Our combined model predicted 138 lakes within British Columbia to be at high risk of smallmouth bass introduction, raising the question how widespread this invader might become in a province containing over 67,000 lakes. Once smallmouth bass has been introduced into a lake, there is a clear risk of further spread through natural dispersal within the watershed, illustrated by the high ratio of lakes predicted as environmentally suitable (38.6%) in British Columbia. Hence, smallmouth bass has the potential to become a widespread invader across British Columbia, with potential negative impacts on a whole range of native freshwater species and communities. We acknowledge that we only provide a basic estimate of the potential impact of smallmouth bass invasion on native species. Our estimates would improve with detailed information on the interactions between smallmouth bass and each of the native fish species in British Columbia lakes. Despite the uncertainty, the quantification of smallmouth bass impacts on native species is useful for highlighting the potential severity of smallmouth bass invasion on native ecosystems. CONCLUSIONS Our study incorporated effective predictive models essential to further understanding potential for introduction, establishment and impacts of non-indigenous species, essential to the effective management of non-indigenous species (Vander Zanden & Olden, 2008). Only through informed decisionmaking processes can prevention and control measures be effective. While currently the distribution of smallmouth bass is limited in British Columbia, increased rates of introduction and global climate change can dramatically increase the spread of this species throughout British Columbia and North America (Sharma et al., 2007; Sharma & Jackson, 2008). Currently, the range expansion of bass in North America has been facilitated by stocking by governmental agencies, unauthorized and accidental introduction by anglers, and natural dispersal through drainage networks (Jackson, 2002; Vander Zanden et al., 2004). Our study highlights the possibility of identifying lakes at high risk of future introduction, thereby allowing focused research and management efforts in these systems. The spread of smallmouth bass is largely a result of anthropogenic activities, therefore intensifying public education and regulations will help limit the potential consequences of non-indigenous species on native aquatic communities. ACKNOWLEDGEMENTS We would like to express our thanks to B. Runciman, N. Mandrak, E. Parkinson and K. Minns for fish distribution and environmental data. We would also like to thank Don Jackson for discussion. Our thanks to Associate Editor, T. Ricciardi and two anonymous referees for comments. L.M.H. is funded by an NSERC visiting post-doctoral fellowship.

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S.S. is funded by a University of Toronto Fellowship and a GRIL (Groupe de Recherche Interuniversitaire en Limnologie) Fellowship. REFERENCES Bennett, D.H., Chandler, J.A. & Dunsmoor, L.K. (1991) Smallmouth bass in the Pacific Northwest: benefit or liability. Proceeding of the first international smallmouth bass symposium (ed. by D.C. Jackson), pp. 126–135. Mississippi Agricultural and Forestry Experiment Station, Mississippi State University, Starkville, MS. Bossenbroek, J.M., Kraft, C.E. & Nekola, J.C. (2001) Prediction of long-distance dispersal using gravity models: zebra mussel invasion of inland lakes. Ecological Applications, 11, 1778– 1788. Casselman, J.M., Brown, D.M., Hoyle, J.A. & Eckert, T.H. (2002) Effects of climate and global warming on year-class strength and relative abundance of smallmouth bass in eastern Lake Ontario. Black Bass: ecology, conservation and management (ed. by D.P. Philipp and M.S. Ridgway), pp. 73–90. American Fisheries Society Symposium 31, Bethesda, MD. Colautti, R.I. & MacIsaac, H.J. (2004) A neutral terminology to define ‘invasive’ species. Diversity and Distributions, 10, 135– 141. De’ath, G. & Fabricius, K.E. (2000) Classification and regression trees: a powerful yet simple technique for ecological data analysis. Ecology, 81, 3178–3192. Drake, J.M. & Bossenbroek, J.M. (2004) The potential distribution of zebra mussels in the United States. BioScience, 54, 931–941. Drake, J.M. & Lodge, D.M. (2007) Rate of species introductions in the Great Lakes via ships’ ballast water and sediments. Canadian Journal of Fisheries and Aquatic Sciences, 64, 530–538. Dunlop, E.S. & Shuter, B.J. (2006) Native and introduced populations of smallmouth bass differ in concordance between climate and somatic growth. Transactions of the American Fisheries Society, 135, 1175–1190. Fielding, A.H. & Bell, J.F. (1997) A review of methods for the assessment of prediction errors in conservation presence/ absence models. Environmental Conservation, 24, 38–49. Findlay, C.S., Bert, D.G. & Zheng, L. (2000) Effect of introduced piscivores on native minnow communities in Adirondack lakes. Canadian Journal of Fisheries and Aquatic Sciences, 57, 570–580. Fritts, A.L. & Pearsons, T.N. (2004) Smallmouth bass predation on hatchery and wild salmonids in the Yakima River, Washington. Transactions of the American Fisheries Society, 133, 880–895. Fritts, A.L. & Pearsons, T.N. (2006) Effects of predation by nonnative smallmouth bass on native salmonid prey: the role of predator and prey size. Transactions of the American Fisheries Society, 135, 853–860.

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Predicting the invasion of smallmouth bass Guisan, A. & Thuiller, W. (2005) Predicting species distribution: offering more than simple habitat models. Ecology Letters, 8, 993–1009. Harvey, H.H. (1981) Fish communities of the lakes of the Bruce Penninsula. Internationale Vereinigung fur Theoretische und Angewandte Limnologie Verhandlungen, 21, 1222– 1230. Harvey, C.J. & Kareiva, P.M. (2005) Community context and the influence of non-indigenous species on juvenile salmon survival in a Columbia River reservoir. Biological Invasions, 7, 651–663. Herborg, L.M., Jerde, C.J., Lodge, D.M., Ruiz, G.M. & MacIsaac, H.J. (2007a) Predicting invasion risk using measures of introduction effort and environmental niche models. Ecological Applications, 17, 663–674. Herborg, L.M., Mandrak, N.E., Cudmore, B. & MacIsaac, H.J. (2007b) Comparative distribution and invasion risk of snakehead and Asian carp species in North America. Canadian Journal of Fisheries and Aquatic Sciences, 64, 1723–1735. Jackson, D.A. (2002) Ecological effects of Micropterus introductions: the dark side of black bass. Black Bass: ecology, conservation and management (ed. by D.P. Philipp and M.S. Ridgway), pp. 221–232. American Fisheries Society Symposium 31, Bethesda, MD. Jackson, D.A. & Mandrak, N.E. (2002) Changing fish biodiversity: predicting the loss of cyprinid biodiversity due to global climate change. Fisheries in a changing climate (ed. by N.A. McGinn), pp. 89–98. American Fisheries Society Symposium 32, Bethesda, MD. Johnson, L.E., Ricciardi, A. & Carlton, J.T. (2001) Overland dispersal of aquatic invasive species: a risk assessment of transient recreational boating. Ecological Applications, 11, 1789–1799. Kraft, C.E. & Johnson, L.E. (2000) Regional differences in rates and patterns of North American inland lake invasions by zebra mussels (Dreissena polymorpha). Canadian Journal of Fisheries and Aquatic Sciences, 57, 993–1001. Leung, B. & Mandrak, N.E. (2007) The risk of establishment of aquatic invasive species: joining invasibility and propagule pressure. Proceedings of the Royal Society B: Biological Sciences, 274, 2603–2609. Leung, B., Bossenbroek, J.M. & Lodge, D.M. (2006) Boats, pathways, and aquatic biological invasions: estimating dispersal potential with gravity models. Biological Invasions, 8, 241–254. Lodge, D.M. & Shrader-Frechette, K. (2003) Nonindigenous species: ecological explanation, environmental ethics, and public policy. Conservation Biology, 17, 31–37. MacIsaac, H.J., Borbely, J.V.M., Muirhead, J.R. & Graniero, P.A. (2004) Backcasting and forecasting biological invasions of inland lakes. Ecological Applications, 14, 773–783. MacRae, P.S.D. & Jackson, D.A. (2001) The influence of smallmouth bass (Micropterus dolomieu) predation and habitat complexity on the structure of littoral zone fish assemblages. Canadian Journal of Fisheries and Aquatic Sciences, 58, 342–351.

Minns, C.K. (1986) A model of bias in lake selection for survey. Canadian Technical Report of Fisheries and Aquatic Sciences, 1496, 1–21. Muirhead, J.R. & MacIsaac, H.J. (2005) Development of inland lakes as hubs in an invasion network. Journal of Applied Ecology, 42, 80–90. Muirhead, J.R., Leung, B., van Overdijk, C., Kelly, D.W., Nandakumar, K., Marchant, K.R. & MacIsaac, H.J. (2006) Modelling local and long-distance dispersal of invasive emerald ash borer Agrilus planipennis (Coleoptera) in North America. Diversity and Distributions, 12, 71–79. Olden, J.D. & Jackson, D.A. (2002) A comparison of statistical approaches for modeling fish species distributions. Freshwater Biology, 10, 1976–1995. Olver, C.H., Desjardine, R.L., Goddard, C.I., Powell, M.J., Reitveld, H.J. & Waring, P.D. (1991) Lake trout in Ontario: management strategies. Ontario Ministry of Natural Resources, Lake Trout Synthesis, Toronto. Pimentel, D., Lach, L., Zuniga, R. & Morrison, D. (2005) Update on the environmental and economic costs associated with alien invasive species in the United States. Ecological Economics, 52, 273–288. Rahel, F.J. (2000) Homogenization of fish faunas across the United States. Science, 288, 854–856. Rahel, F.J. (2007) Biogeographic barriers, connectivity and homogenization of freshwater faunas: it’s a small world after all. Freshwater Biology, 52, 696–710. Reed-Andersen, R., Carpenter, S.R., Padilla, D.K. & Lathrop, R.C. (2000) Predicted impact of zebra mussel (Dreissena polymorpha) invasion on water clarity in Lake Mendota. Canadian Journal of Fisheries and Aquatic Sciences, 57, 1617– 1626. Ricciardi, A. & MacIsaac, H.J. (2000) Recent mass invasion of the North American Great Lakes by Ponto-Caspian species. Trends in Ecology and Evolution, 15, 62–65. Rouget, M. & Richardson, D.M. (2003) Inferring process from pattern in plant invasions: a semimechanistic model incorporating propagule pressure and environmental factors. The American Naturalist, 162, 713–724. Sala, O.E., Chapin, F.S., Armesto, J.J., Berlow, E., Bloompeld, J., Dirzo, R., Huber-Sanwald, E., Huenneke, L.F., Jackson, R.B., Kinzig, A., Leemans, R., Lodge, D.M., Mooney, H.A., Oesterheld, M., Poff, N.L., Sykes, M.T., Walker, B.H., Walker, M. & Wall, D.H. (2000) Global biodiversity scenarios for the year 2100. Science, 287, 1770–1774. Scott, W.B. & Crossman, E.J. (1998) Freshwater fishes of Canada. Fisheries Research Board of Canada, Ottawa, ON, Canada. Sharma, S. & Jackson, D.A. (2008) Predicting smallmouth bass occurrence across North America: a comparison of statistical approaches. Canadian Journal of Fisheries and Aquatic Sciences, 65, 471–481. Sharma, S., Jackson, D.A., Minns, C.K. & Shuter, B.J. (2007) Will northern fish populations be in hot water because of climate change? Global Change Biology, 13, 1052–1064. Sharma, S., Jackson, D.A. & Minns, C.K. (in press) Quantifying the potential effects of climate change and the invasion of

Diversity and Distributions, 15, 831–840, ª 2009 Blackwell Publishing Ltd

839

S. Sharma et al. smallmouth bass on native lake trout populations across Canadian lakes. Ecography. doi: 10.1111/j.0906-7590. 2008.05544.x. Shuter, B.J. & Ridgway, M.S. (2002) Bass in time and space: operational definitions of risk. Black Bass: ecology, conservation and management (ed. by D.P. Philipp and M.S. Ridgway), pp. 235–249. American Fisheries Society Symposium 31, Bethesda, MD. Shuter, B.J., MacLean, J.A., Fry, F.E.J. & Regier, H.A. (1980) Stochastic simulation of temperature effects on first-year survival of smallmouth bass. Transactions of the American Fisheries Society, 109, 1–34. Simberloff, D., Parker, I.M. & Windle, P.N. (2005) Introduced species policy, management, and future research needs. Frontiers in Ecology and the Environment, 3, 12–20. Tabor, R.A. & Wurtsbaugh, W.A. (1991) Predation risk and the importance of cover for juvenile rainbow trout in lentic systems. Transactions of the American Fisheries Society, 120, 728–738. Tonn, W.M. & Magnuson, J.J. (1982) Patterns in the species composition and richness of fish assemblages in northern Wisconsin lakes. Ecology, 63, 1149–1166. Vander Zanden, M.J. & Olden, J.D. (2008) A management framework for preventing the secondary spread of aquatic invasive species. Canadian Journal of Fisheries and Aquatic Sciences, 65, 1512–1522. Vander Zanden, M.J., Casselman, J.M. & Rasmussen, J.B. (1999) Stable isotope evidence for the food web consequences of species invasions in lakes. Nature, 401, 464– 467.

840

Vander Zanden, M.J., Olden, J.D., Thorne, J.H. & Mandrak, N.E. (2004) Predicting occurrences and impacts of smallmouth bass introduction in north temperate lakes. Ecological Applications, 14, 132–148. Wismer, D.A., DeAngelis, D.L. & Shuter, B.J. (1985) An empirical model of size distributions of smallmouth bass. Transactions of the American Fisheries Society, 114, 737–742. Wonham, M.J., Bailey, S.A., MacIsaac, H.J. & Lewis, D.B. (2005) Modelling the invasion risk of diapausing organisms transported in ballast sediments. Canadian Journal of Fisheries and Aquatic Sciences, 62, 2386–2398. Editor: Anthony Ricciardi

SUPPORTING INFORMATION Additional Supporting Information may be found in the online version of this article: Appendix S1 Models predicting the occurrence of smallmouth bass. Appendix S2 Lakes identified at risk to smallmouth bass introduction and establishment in British Columbia. Please note: Wiley-Blackwell is not responsible for the content or functionality of any supporting materials supplied by the authors. Any queries (other than missing material) should be directed to the corresponding author for the article.

Diversity and Distributions, 15, 831–840, ª 2009 Blackwell Publishing Ltd