A Global Review and Meta-Analysis of Applications of the Freshwater Fish Invasiveness Screening Kit
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A global review and meta-analysis of applications of the freshwater Fish Invasiveness Screening Kit Lorenzo Vilizzi, Gordon H. Copp, Boris Adamovich, David Almeida, Joleen Chan, Phil I. Davison, Samuel Dembski, F. Güler Ekmekçi, et al. Reviews in Fish Biology and Fisheries ISSN 0960-3166 Rev Fish Biol Fisheries DOI 10.1007/s11160-019-09562-2 1 23 Your article is published under the Creative Commons Attribution license which allows users to read, copy, distribute and make derivative works, as long as the author of the original work is cited. You may self- archive this article on your own website, an institutional repository or funder’s repository and make it publicly available immediately. 1 23 Rev Fish Biol Fisheries https://doi.org/10.1007/s11160-019-09562-2 (0123456789().,-volV)( 0123456789().,-volV) REVIEWS A global review and meta-analysis of applications of the freshwater Fish Invasiveness Screening Kit Lorenzo Vilizzi . Gordon H. Copp . Boris Adamovich . David Almeida . Joleen Chan . Phil I. Davison . Samuel Dembski . F. Gu¨ler Ekmekc¸i . A´ rpa´d Ferincz . Sandra C. Forneck . Jeffrey E. Hill . Jeong-Eun Kim . Nicholas Koutsikos . Rob S. E. W. Leuven . Sergio A. Luna . Filomena Magalha˜es . Sean M. Marr . Roberto Mendoza . Carlos F. Moura˜o . J. Wesley Neal . Norio Onikura . Costas Perdikaris . Marina Piria . Nicolas Poulet . Riikka Puntila . Ineˆs L. Range . Predrag Simonovic´ . Filipe Ribeiro . Ali Serhan Tarkan . De´bora F. A. Troca . Leonidas Vardakas . Hugo Verreycken . Lizaveta Vintsek . Olaf L. F. Weyl . Darren C. J. Yeo . Yiwen Zeng Received: 10 January 2019 / Accepted: 17 April 2019 Ó The Author(s) 2019 Abstract The freshwater Fish Invasiveness Screen- FISK applications and the confidence (certainty) ing Kit (FISK) has been applied in 35 risk assessment levels associated with the decision-support tool’s 49 areas in 45 countries across the six inhabited conti- questions and its ability to distinguish between taxa of nents (11 applications using FISK v1; 25 using FISK low-to-medium and high risk of becoming invasive, v2). The present study aimed: to assess the breadth of and thus provide climate-specific, generalised, cali- brated thresholds for risk level categorisation; and to identify the most potentially invasive freshwater fish Electronic supplementary material The online version of species on a global level. The 1973 risk assessments this article (https://doi.org/10.1007/s11160-019-09562-2) con- were carried out by 70 ? experts on 372 taxa (47 of tains supplementary material, which is available to authorized users. L. Vilizzi (&) Á G. H. Copp Á A. S. Tarkan B. Adamovich Department of Ecology and Vertebrate Zoology, Faculty Faculty of Biology, Belarusian State University, Minsk, of Biology and Environmental Protection, University of Belarus Ło´dz´,Ło´dz´, Poland e-mail: [email protected] D. Almeida Departamento de Ciencias Me´dicas Ba´sicas, Facultad de G. H. Copp Á P. I. Davison Medicina, Universidad San Pablo-CEU, Madrid, Spain Centre for Environment, Fisheries and Aquaculture Science, Lowestoft, UK J. Chan Á D. C. J. Yeo Á Y. Zeng Department of Biological Sciences, National University G. H. Copp of Singapore, Singapore, Singapore Department of Life and Environmental Sciences, Bournemouth University, Poole, UK S. Dembski Agence Franc¸aise pour la Biodiversite´, Vincennes, France G. H. Copp Environmental and Life Sciences Graduate Program, F. G. Ekmekc¸i Trent University, Peterborough, Canada Hydrobiology Section, Biology Department, Faculty of Science, Hacettepe University, Ankara, Turkey 123 Rev Fish Biol Fisheries the 51 species listed as invasive in the Global Invasive interest and therefore warrant a full, comprehensive Species Database www.iucngisd.org/gisd/), which RA to assess their potential adverse impacts on native in decreasing order of importance belonged to species and ecosystems (Ricciardi and Rasmussen the taxonomic Orders Cypriniformes, Perciformes, 1998; Copp et al. 2005a, b). The development of risk Siluriformes, Characiformes, Salmoniformes, analysis protocols for aquatic NNS in recent decades Cyprinodontiformes, with the remaining & 8% of has been strongly influenced by decision-support (DS) taxa distributed across an additional 13 orders. The tools developed for the analysis of weeds and plant most widely-screened species (in decreasing impor- pests (see Baker et al. 2005), with perhaps the most tance) were: grass carp Ctenopharyngodon idella, widely-used risk identification tools being the Weed common carp Cyprinus carpio, rainbow trout On- Risk Assessment (WRA) for non-native terrestrial corhynchus mykiss, silver carp Hypophthalmichthys plants (Pheloung et al. 1999) and its direct derivative, molitrix and topmouth gudgeon Pseudorasbora parva. the Fish Invasiveness Screening Kit (FISK) for Nine ‘globally’ high risk species were identified: freshwater fishes (Copp et al. 2005a, b)—sometimes common carp, black bullhead Ameiurus melas, round also referred to, albeit less correctly, as the Fish goby Neogobius melanostomus, Chinese (Amur) Invasiveness Scoring Kit (e.g. Gozlan et al. 2010; sleeper Perccottus glenii, brown bullhead Ameiurus Onikura et al. 2011; Tricarico et al. 2010; Verbrugge nebulosus, eastern mosquitofish Gambusia holbrooki, et al. 2012; Lawson et al. 2013; Puntila et al. 2013; largemouth (black) bass Micropterus salmoides, Vilizzi and Copp 2013). pumpkinseed Lepomis gibbosus and pikeperch Sander A user-friendly DS tool based in ExcelÒ, the WRA lucioperca. The relevance of this global review to had been applied globally (Gordon et al. 2008) prior to policy, legislation, and risk assessment and manage- its adaptation in 2005 (Copp et al. 2005a, b) to create ment procedures is discussed. FISK and its sister ‘-ISK’ toolkits for freshwater invertebrates (FI-ISK), marine fish (MFISK), marine Keywords Decision support tools Á FISK Á Hazard invertebrates (MI-ISK) and amphibians (Amph-ISK). identification Á Ko¨ppen-Geiger climate Á Non-native The first application and calibration of these screening species Á Risk analysis tools was with FISK v1 to identify potentially invasive freshwater fishes in England & Wales (Copp et al. 2009). This DS tool was subsequently applied to several RA areas in Europe, Asia, North and South Introduction America (Copp 2013; Table 1), before being replaced by a much improved version (v2: Lawson et al. 2013). The first, and crucial, step in non-native species (NNS) Global applications of FISK v1 and v2 include RA risk analysis is to identify which species are likely to areas in the six inhabited continents (see Table 1), become invasive in the risk assessment (RA) area of A´ . Ferincz J.-E. Kim Department of Aquaculture, Faculty of Agricultural and College of Bioscience and Biotechnology, Chungnam Environmental Sciences, Szent Istva´n University, National University, Daejeon, Republic of Korea Go¨do¨llo,} Hungary N. Koutsikos Á L. Vardakas S. C. Forneck Hellenic Centre for Marine Research, Institute of Marine Laborato´rio de Ecologia, Pesca e Ictiologia, Universidade Biological Resources and Inland Waters, Federal do Parana´, Palotina, Brazil Anavissos, Attica, Greece S. C. Forneck R. S. E. W. Leuven Laborato´rio de Ecologia e Conservac¸a˜o, Universidade Department of Animal Ecology and Physiology, Institute Federal do Parana´, Curitiba, Brazil for Water and Wetland Research, Radboud University, Nijmegen, The Netherlands J. E. Hill Tropical Aquaculture Laboratory, Program in Fisheries and Aquatic Sciences, School of Forest Resources and Conservation, University of Florida, Ruskin, FL, USA 123 Rev Fish Biol Fisheries which contrasts the more limited geographical appli- assess the capability of FISK as a screening DS tool to cation of the other ‘-ISK’ tools, i.e. FI-ISK (Tricarico distinguish correctly between non-invasive and inva- et al. 2010; Urho et al. 2012; Chucholl 2013;Sˇkraba sive taxa and categorise them according to risk level; et al. 2013; Papavlasopoulou et al. 2014; Patoka et al. and (iv) provide climate-specific, generalised thresh- 2014; Loureiro et al. 2015; Kotovska et al. 2016; olds for risk level categorisation so as to identify the Tovar Herna´ndez 2016; Chucholl and Wendler 2017; most potentially invasive species on a global level. It is Patoka et al. 2017; Uderbayev et al. 2017; Vodovsky anticipated that the findings of the present study will et al. 2017; Weiperth et al. 2018), MFISK (Copp et al. reveal the robustness of FISK as a DS tool, as well as 2013), MI-ISK (Drolet et al. 2016; Perdikaris et al. similarities and differences in thresholds and scores 2016a), and AmphISK (Kopecky´ et al. 2016). depending on RA areas. Identifying such generalis- An initial summary of these applications (Copp ations and specificities within FISK will help improve 2013) reported calibrated thresholds to distinguish its accuracy and enable better-informed and more between the categories of low-to-medium and high effective management strategies for the management risk of the screened species becoming invasive in the and conservation of freshwater ecosystems. Finally, RA area, which henceforth are referred to as medium- the global and climate-specific thresholds identified in and high-risk species. Also, Copp’s (2013) summary the present study will contribute to the transferability emphasised the importance of screening species and calibration of thresholds to be developed for the within the context of a defined RA area and recom- AS-ISK tool, and the evaluation of a wide range of mended that species assessments should ideally be FISK applications will