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Effectiveness of FISK, an Invasiveness Screening Tool for Nonnative

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Effectiveness of FISK, an Invasiveness Screening Tool for Nonnative Risk Analysis DOI: 10.1111/risa.12050 Effectiveness of FISK, an Invasiveness Screening Tool for Non-Native Freshwater Fishes, to Perform Risk Identification Assessments in the Iberian Peninsula David Almeida,1,2 Filipe Ribeiro,3,4 Pedro M. Leunda,5,6 Lorenzo Vilizzi,7 and Gordon H. Copp1,2,6,8,∗ Risk assessments are crucial for identifying and mitigating impacts from biological invasions. The Fish Invasiveness Scoring Kit (FISK) is a risk identification (screening) tool for fresh- water fishes consisting of two subject areas: biogeography/history and biology/ecology. Ac- cording to the outcomes, species can be classified under particular risk categories. The aim of this study was to apply FISK to the Iberian Peninsula, a Mediterranean climate region highly important for freshwater fish conservation due to a high level of endemism. In total, 89 fish species were assessed by three independent assessors. Results from receiver operating characteristic analysis showed that FISK can discriminate reliably between noninvasive and invasive fishes for Iberia, with a threshold of 20.25, similar to those obtained in several regions around the world. Based on mean scores, no species was categorized as “low risk,” 50 species as “medium risk,” 17 as “moderately high risk,” 11 as “high risk,” and 11 as “very high risk.” The highest scoring species was goldfish Carassius auratus. Mean certainty in response was above the category “mostly certain,” ranging from tinfoil barb Barbonymus schwanenfeldii with the lowest certainty to eastern mosquitofish Gambusia holbrooki with the highest level. Pair-wise comparison showed significant differences between one assessor and the other two on mean certainty, with these two assessors showing a high coincidence rate for the species categorization. Overall, the results suggest that FISK is a useful and viable tool for assessing risks posed by non-native fish in the Iberian Peninsula and contributes to a “watch list” in this region. KEY WORDS: Alien species prescreening; aquatic conservation; biological invasions; hazard identification 1. INTRODUCTION 1Salmon & Freshwater Team, Cefas, Pakefield Road, Lowestoft, The Iberian Peninsula has a unique freshwater Suffolk, NR33 0HT, UK. fish fauna with a high level of endemism, that is, 2 Centre for Conservation Ecology, Bournemouth University, >30% of native species,(1–4) and is increasingly Poole, Dorset, BH12 5BB, UK. 3Centro de Oceanografia, Faculdade de Cienciasˆ da Universidade threatened by human-mediated pressures such as de Lisboa, Campo Grande 1749-016 Lisboa, Portugal. 4Museu Nacional de Historia´ Natural e da Ciencia,ˆ Universi- dade de Lisboa, Rua da Escola Politecnica´ 58, 1269-102 Lisboa, 7Murray-Darling Freshwater Research Centre, PO Box 991, Portugal. Wodonga VIC 3689, Australia. 5Gestion´ Ambiental de Navarra S.A., C/ Padre Adoain 219 Bajo, 8Environmental and Life Sciences Graduate Program, Trent Uni- 31015 Pamplona/Iruna,˜ Navarra, Espana.˜ versity, Peterborough, Ontario K9J 7B8, Canada. 6University of Navarra, School of Sciences, Department of En- ∗Address correspondence to Gordon H. Copp, Salmon & vironmental Biology,, c/Irunlarrea 1, E-31008, Pamplona/Iruna,˜ Freshwater Team, Cefas, Pakefield Road, Lowestoft, Suffolk Navarra, Spain. NR33 OHT, UK; [email protected]. 1 0272-4332/13/0100-0001$22.00/1 C 2013 Society for Risk Analysis 2 Almeida et al. water extraction, pollution, discharge regulation, and encompass all stages of the invasion process.(24) non-native species.(5) In Europe, several countries Details on the weighting of outcome scores, which show high ratios of non-native fishes, such as Greece range from −15 to 57, with which to rank the poten- (19%),(6) the United Kingdom (21%),(7) or the tial risk of a species being invasive as low, medium, Czech Republic (23%).(8) Currently, the Iberian or high are described in detail elsewhere.(25) Peninsula is considered a non-native species hotspot The aim of this study was to undertake a risk for freshwater fishes, that is, >25% of total fish identification assessment of non-native fishes rele- species are non-native,(9) where non-native fishes vant to Iberian drainage basins, and thus contribute can exert a range of impacts on native ecosystems, to the broader geographic applicability of the FISK. including predation, competition, habitat alteration, Relevant species include existing translocated and hybridization, and disease transmission.(9,10) Yet, the non-native fishes, as well as possible future invaders number of non-native fishes in the Iberian Peninsula of the peninsula. continues to increase despite concerns that these pose an increasing threat to biodiversity.(11,12) Thus, assessments of non-native fish risks are essential for 2. METHODOLOGY controlling their numbers and thus mitigating their potential impacts.(13) A total of 89 fish species (Table I) was assessed To evaluate invasion risks in the Iberian Penin- with FISK v2.(21) The selection of species was based sula, most of the conducted research has focused on the following criteria: (i) native species from the on identifying key biological traits that facilitate Iberian Peninsula that have been translocated across successful fish invasions.(14,15) Recently, a risk assess- Iberian watersheds into drainage basins outside their ment approach has been proposed for non-native native range; (ii) non-native species already present fishes in the Iberian Peninsula(12) that is dependent in the Iberian Peninsula that could spread into new on a profound understanding of invasion pathways Iberian areas; (iii) non-native species that are cur- and detailed knowledge of the key biological fea- rently not present in the Iberian Peninsula but are tures that determine invasion success in this region. located near the “Perpignan corridor”—a recognized In aiming to aid in the prevention of future intro- “donor area” of fish introductions to the Iberian ductions, the Clavero(12) approach focused mainly Peninsula;(26) and (iv) non-native species that are not on early invasion stages (i.e., arrival and establish- currently present either in the Iberian Peninsula or ment), and was less comprehensive regarding risks near the Perpignan corridor but are important for associated with the subsequent dispersal and impact aquaculture or the aquarium trade. Of the 89 fish stages of the invasion process. Furthermore, the species, 16 (18.0%) were classified according to cri- Clavero approach(12) followed a region-specific pro- terion (i), 25 (28.1%) as per criterion (ii), 34 (38.2%) cedure that is not easily applied outside the Iberian as per criterion (iii), and the remaining 14 (15.7%) as Peninsula, thus limiting its use to inform man- per criterion (iv). agers and policymakers in a broader context (e.g., Receiver operating characteristic (ROC) European legislation). analysis(27) was used to assess the predictive ability This contrasts the Fish Invasiveness Scoring Kit of FISK to discriminate between invasive and non- (FISK), which is a risk identification (screening) invasive species. To this end, species were classified tool that has been successfully applied in differ- apriorias either invasive or noninvasive based on ent countries around the globe(16–20) and recently information available from the Invasive Species revised for wider use, including warm temperate Specialist Group Database (http://www.issg.org/) and subtropical climatic zones, such as peninsular and from FishBase (http://www.fishbase.org). Sta- Florida, United States.(21) Adapted from the Weed tistically, an ROC curve is a graph of sensitivity Risk Assessment(22) by Copp et al.(23) for assessing versus 1 – specificity (or alternatively, sensitivity vs. non-native freshwater fishes in the United King- specificity), where in the present context sensitivity dom, FISK consists of 49 questions that address and specificity will be the proportion of invasive eight topics (domestication/cultivation, climate and and noninvasive fish species, respectively, that are distribution, invasive elsewhere, undesirable traits, correctly identified by the FISK tool as such. A feeding guild, reproduction, dispersal mechanisms, measure of the accuracy of the calibration analysis and persistence attributes) under two main subject is the area under the ROC curve (AUC). If the areas (biogeography/history, biology/ecology) that AUC is equal to 1.0 (i.e., the ROC “curve” consists Effectiveness of FISK for Assessing Fishes in Iberia 3 Table I. Fish Species Assessed with FISK v2 for the Iberian Peninsula Score CF Invasiveness/ Species Name Common Name Criterion Protection Status Mean Min Max SE Outcome Mean Min Max SE Abramis brama common bream 2 Noninvasive/LC 23.2 20.0 26.5 1.9 MH 0.79 0.73 0.84 0.03 Achondrostoma arcasii bermejuela 1 Noninvasive/VU 5.7 0.0 9.0 2.8 M 0.86 0.76 0.92 0.05 Acipenser baerii Siberian sturgeon 3 Noninvasive/NE 11.5 9.0 13.0 1.3 M 0.82 0.78 0.86 0.02 Acipenser naccarii Adriatic sturgeon 4 Noninvasive/CR 8.0 5.0 10.0 1.5 M 0.81 0.75 0.87 0.04 Alburnoides bipunctatus spirlin 3 Noninvasive/NE 6.7 2.0 9.0 2.3 M 0.76 0.68 0.85 0.05 Alburnus alburnus bleak 2 Noninvasive/LC 25.3 20.0 31.0 3.2 H 0.85 0.75 0.90 0.05 Ameiurus melas black bullhead 2 Invasive/NE 32.7 27.0 36.0 2.8 VH 0.84 0.78 0.92 0.04 Anguilla anguilla European eel 1 Noninvasive/CR 20.0 11.0 26.0 4.6 M 0.89 0.80 0.94 0.05 Aphanius fasciatus southern-European toothcarp 3 Noninvasive/LC 10.3 8.0 13.0 1.5 M 0.74 0.65 0.89 0.07 Astronotus ocellatus oscar 4 Noninvasive/NE 16.5 11.0 19.5 2.8 M 0.74 0.64 0.83 0.05 Australoheros facetus chameleon cichlid 2 Noninvasive/NE
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