A multi-taxa assessment of aquatic non-indigenous species introduced into Iberian freshwater and transitional waters

A multi-taxa assessment of aquatic non-indigenous species introduced into Iberian freshwater and transitional waters Jose M. Zamora-Marín1,2, Ana Ruiz-Navarro1,3, Francisco J. Oficialdegui1,4, Pedro M. Anastácio5, Rafael Miranda6, Pablo García-Murillo7, Fernando Cobo8, Filipe Ribeiro9, Belinda Gallardo10, Emili García-Berthou11, Dani Boix11, Leopoldo Medina12, Felipe Morcillo13, Javier Oscoz6, Antonio Guillén1, Antonio A. Herrero-Reyes1, Francisca C. Aguiar14, David Almeida15, Andrés Arias16, César Ayres17, Filipe Banha5, Sandra Barca8, Idoia Biurrun18, M. Pilar Cabezas19, Sara Calero20, Juan A. Campos18, Laura Capdevila-Argüelles21, César Capinha22,23, André Carapeto24, Frederic Casals25,26, Paula Chainho9, Santos Cirujano27, Miguel Clavero28, Jose A. Cuesta29, Vicente Deltoro30, João Encarnação31, Carlos Fernández-Delgado32, Javier Franco33, Antonio J. García-Meseguer34, Simone Guareschi28, Adrián Guerrero-Gómez1, Virgilio Hermoso7, Celia López-Cañizares1, Joaquín López-Soriano35, Annie Machordom36, Joana Martelo9, Andrés Mellado-Díaz20, Juan C. Moreno37, Rosa Olivo del Amo1, J. Carlos Otero8, Anabel Perdices36, Quim Pou-Rovira38, Sergio Quiñonero-Salgado35, Argantonio Rodríguez-Merino7, Macarena Ros39, Enrique Sánchez-Gullón40, Marta I. Sánchez41, David Sánchez-Fernández34, Jorge R. Sánchez-González42, Oscar Soriano36, M. Alexandra Teodósio31, Mar Torralva1, Rufino Vieira-Lanero8, Antonio Zamora-López1, Francisco J. Oliva-Paterna1 1Department of Zoology and Physical Anthropology, Faculty of Biology, University of Murcia, CEIR Campus Mare Nostrum (CMN), Murcia, Spain 2Department of Applied Biology, Centro de Investigación e Innovación Agroalimentaria (CIAGRO-UMH), Miguel Hernández University of Elche, Elche, Spain 3Department of Didactics on Experimental Sciences, Faculty of Education, University of Murcia, Murcia, Spain 4University of South Bohemia in České Budějovice, Faculty of Fisheries and Protection of Waters, South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses, Zátiší 728/II, 389 25 Vodňany, Czech Republic 5MARE – Centro de Ciências do Mar e do Ambiente, Departamento de Paisagem, Ambiente e Ordenamento, Escola de Ciências e Tecnologia, Universidade de Évora, Évora, Portugal 6Instituto de Biodiversidad y Medioambiente (BIOMA), Universidad de Navarra, Pamplona, Spain 7Departamento de Biología Vegetal y Ecología, Facultad de Farmacia, Universidad de Sevilla, Sevilla, Spain 8Departamento de Zooloxía, Xenética e Antropoloxía Física, Facultade de Bioloxía, Universidade de Santiago de Compostela, A Coruña, Spain 9MARE – Centro de Ciências do Mar e do Ambiente, Faculdade de Ciências NeoBiota 89: 17–44 (2023) doi: 10.3897/neobiota.89.105994 https://neobiota.pensoft.net Copyright Jose M. Zamora-Marín et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. RESEARCH ARTICLE Advancing research on alien species and biological invasions A peer-reviewed open-access journal NeoBiota Jose M. Zamora-Marín et al. / NeoBiota 89: 17–44 (2023) 18 da Universidade de Lisboa, Lisboa, Portugal 10Instituto Pirenaico de Ecología (IPE), CSIC, Zaragoza, Spain 11GRECO, Institute of Aquatic Ecology, University of Girona, Girona, Spain 12Sistemática de Plantas Vasculares, Real Jardín Botánico (RJB-CSIC), Madrid, Spain 13Departamento de Biodiversidad, Ecología y Evolución, Universidad Complutense de Madrid, Madrid, Spain 14Centro de Estudos Florestais, Instituto Superior de Agronomia, Universidade de Lisboa, Lisboa, Portugal 15Department of Basic Medical Sciences, School of Medicine, Universidad San Pablo-CEU, CEU Universities, Madrid, Spain 16Departamento de Biología de Organismos y Sistemas, Universidad de Oviedo, Oviedo, Asturias, Spain 17Asociación Herpetológica Española (A.H.E.), Museo Nacional de Ciencias Naturales (MNCNCSIC), Madrid, Spain 18Department of Plant Biology and Ecology, University of the Basque Country UPV/EHU, Bilbao, Spain 19Department of Biogeographical Ecology and Evolution, Centro de Ciências do Mar (CCMAR), Universidade do Algarve, Faro, Portugal 20Tragsatec, TSUP Planificación y Gestión Hídrica, Grupo Tragsa – SEPI, Madrid, Spain 21GEIB - Grupo Especialista en Invasiones Biológicas, León, Spain 22Centre of Geographical Studies, Institute of Geography and Spatial Planning, University of Lisbon, 1600-276 Lisboa, Portugal 23Associated Laboratory Terra, Tapada da Ajuda, 1349-017 Lisboa, Portugal 24Coordinador de Lista Vermelha da Flora de Portugal Continental, Sociedade Portuguesa de Botânica, Coimbra, Portugal 25Departament de Ciència Animal, Universitat de Lleida, Lleida, Spain 26Centre Tecnològic Forestal de Catalunya (CTFC), Solsona, Lleida, Spain 27Ecología, conservación de macrófitos acuáticos y cambio global, Real Jardín Botánico (RJB-CSIC), Madrid, Spain 28Departamento de Biología de la Conservación, Estación Biológica de Doñana (EBD-CSIC), Sevilla, Spain 29Departamento de Ecología y Gestión Costera, Instituto de Ciencias Marinas de Andalucía (ICMAN-CSIC), Cádiz, Spain 30Técnico Superior en Medio Ambiente, VAERSA-GVA, Generalitat Valenciana, Valencia, Spain 31CCMAR - Centro de Ciências do Mar, Universidade do Algarve, Algarve, Portugal 32Departamento de Zoología, Universidad de Córdoba, Córdoba, Spain 33AZTI, Investigación Marina, Gestión Ambiental de Mares y Costas, Pasaia, Guipúzkoa, Spain 34Departamento de Ecología e Hidrología, Facultad de Biología, Universidad de Murcia, Murcia, Spain 35Associació Catalana de Malacologia-Museu Blau., Barcelona, Spain 36Departamento de Biodiversidad y Biología Evolutiva, Museo Nacional de Ciencias Naturales (MNCN-CSIC), Madrid, Spain 37Departamento de Biología (Botánica), Facultad de Ciencias, Universidad Autónoma de Madrid, Madrid, Spain 38Sorelló - Estudis al Medi Aquàtic, Girona, Spain 39Departamento de Zoología, Facultad de Biología, Universidad de Sevilla, Sevilla, Spain 40Consejería de Sostenibilidad, Medio Ambiente y Economía Azul, Junta de Andalucía, Huelva, Spain 41Departamento de Ecología de Humedales, Estación Biológica de Doñana (EBD-CSIC), Sevilla, Spain 42SIBIC, Departament de Ciència Animal, Universitat de Lleida, Lleida, Spain Corresponding authors: Jose M. Zamora-Marín ([email protected]); Francisco J. Oliva-Paterna ([email protected]) Academic editor: Jaimie T. A. Dick|Received 11 May 2023|Accepted 11 October 2023|Published 1 November 2023 Citation: Zamora-Marín JM, Ruiz-Navarro A, Oficialdegui FJ, Anastácio PM, Miranda R, García-Murillo P, Cobo F, Ribeiro F, Gallardo B, García-Berthou E, Boix D, Medina L, Morcillo F, Oscoz J, Guillén A, Herrero-Reyes AA, Aguiar FC, Almeida D, Arias A, Ayres C, Banha F, Barca S, Biurrun I, Cabezas MP, Calero S, Campos JA, Capdevila- Argüelles L, Capinha C, Carapeto A, Casals F, Chainho P, Cirujano S, Clavero M, Cuesta JA, Deltoro V, Encarnação J, Fernández-Delgado C, Franco J, García-Meseguer AJ, Guareschi S, Guerrero-Gómez A, Hermoso V, López-Cañizares C, López-Soriano J, Machordom A, Martelo J, Mellado-Díaz A, Moreno JC, Olivo del Amo R, Otero JC, Perdices A, Pou-Rovira Q, Quiñonero-Salgado S, Rodríguez-Merino A, Ros M, Sánchez-Gullón E, Sánchez MI, Sánchez- Fernández D, Sánchez-González JR, Soriano O, Teodósio MA, Torralva M, Vieira-Lanero R, Zamora-López A, Oliva- Paterna FJ (2023) A multi-taxa assessment of aquatic non-indigenous species introduced into Iberian freshwater and transitional waters. NeoBiota 89: 17–44. https://doi.org/10.3897/neobiota.89.105994 Aquatic non-indigenous species in Iberian inland waters 19 Abstract Aquatic ecosystems are particularly vulnerable to the introduction of non-indigenous species (NIS), leading to multi-faceted ecological, economic and health impacts worldwide. The Iberian Peninsula comprises an exceptionally biodiverse Mediterranean region with a high number of threatened and endemic aquatic species, most of them strongly impacted by biological invasions. Following a structured approach that combines a systematic review of available information and expert opinion, we provide a comprehensive and updated multi-taxa inventory of aquatic NIS (fungi, macroalgae, vascular plants, invertebrates and vertebrates) in Iberian inland waters. Moreover, we assess overall patterns in the establishment status, introduction pathways, native range and temporal introduction trends of listed NIS. In addition, we discuss the legal coverage provided by both national (Spanish and Portuguese) and European NIS regulations. We inventoried 326 aquatic NIS in Iberian inland waters, including 215 established, 96 with uncertain establishment status and 15 cryptogenic taxa. Invertebrates (54.6%) and vertebrates (24.5%) were the groups with the highest number of NIS, with Arthropoda, Mollusca, and Chordata being the most represented phyla. Recorded NIS originated from diverse geographic regions, with North and South America being the most frequent. Vertebrates and vascular plants were mostly introduced through intentional pathways (i.e. release and escape), whereas invertebrates and macroalgae arrived mostly through unintentional ways (i.e. contaminant or stowaway). Most of the recorded NIS were introduced in Iberian inland waters over the second half of the 20th century, with a high number of NIS introductions being reported in the 2000s. While only 8% of the recorded NIS appear in the European Union list of Invasive Alien Species of Union concern, around 25% are listed in the Spanish and Portuguese NIS regulations. This study provides the most updated checklist of Iberian aquatic NIS, meeting the requirements set by the EU regulation and providing a baseline for the evaluation of its application. We point out the need for coordinated transnational strategies to properly tackle aquatic invasions across borders of the EU members. Keywords Alien species, checklist, environmental management, estuaries, inland waters, Portugal, regulation, Spain, Western Mediterranean Introduction Compared to terrestrial and marine ecosystems, freshwater and transitional waters (hereafter collectively referred to as inland waters) are especially vulnerable to biological invasions due to their intrinsic environmental features (Moorhouse and Macdonald 2015; McFadden et al. 2023), and the high introduction pressure promoted by the wide range of human activities developed in these aquatic habitats (Reid et al. 2019; Cabral et al. 2020). For instance, inland waters support commercial fisheries, aquaculture, shipping, and diverse recreational activities (e.g. sport fishing or navigation). In addition, inland waters are subject to different human infrastructures such as dams, ditches or water transfer systems (Ojaveer et al. 2018; Anastácio et al. 2019; Bailey et al. 2020). Such human activities are well-known drivers of the introduction and spread of non-indigenous species (hereafter, NIS) (Nunes et al. 2015). As a consequence, there is a growing evidence of major impacts caused by NIS at multiple ecological levels in inland waters, with well-demonstrated detrimental effects on native aquatic biota, ecosystem functions and services (Vilà et al. 2011; Gallardo et al. 2016; Guareschi Jose M. Zamora-Marín et al. / NeoBiota 89: 17–44 (2023) 20 et al. 2021). Under this scenario, management actions are urgently required to slow down the introduction rate of NIS in inland waters, to control populations of already established NIS and to prevent secondary spread towards still non-invaded aquatic ecosystems (Britton et al. 2023). In this context, updated inventories of NIS and comprehensive assessments on introduction pathways, native regions and temporal trends of introductions are fundamental for elucidating the causes and consequences of the invasion process (Seebens et al. 2017; Fuentes et al. 2020). Moreover, NIS management policies should be based on a transnational approach involving coordinated surveillance efforts (Bailey et al. 2020; Capinha et al. 2023). This is especially relevant when neighbouring countries share river basins and, consequently, aquatic ecosystems are largely interconnected. However, legislation and direct management are nowadays mostly implemented at national scale (Anastácio et al. 2019). The Mediterranean basin is one of the major global hotspots of biodiversity, with the Iberian Peninsula comprising a particularly species-rich area and harbouring high numbers of endemic species (Araújo et al. 2007; Buira et al. 2017; Rosso et al. 2018). This is even more evident in the case of the Iberian aquatic biodiversity, which shows outstanding ratios of species singularity and endemicity (Doadrio et al. 2011; Hermoso et al. 2016). For instance, about 80% of freshwater fish, 40% of amphibian and 25% of water beetle species occurring in the Iberian Peninsula are endemic (Doadrio et al. 2011; Hermoso et al. 2016). However, most of these species are highly threatened and particularly vulnerable to NIS introductions (e.g. Cruz et al. 2008; Ruiz-Navarro et al. 2013; Romero 2015). In fact, the introduction of both animal and plant species in Iberian inland waters is a long-lasting and ongoing process, whose adverse effects have been largely documented from an ecological (Aguiar and Ferreira 2013; Anastácio et al. 2019), socioeconomic (Durán et al. 2012; Angulo et al. 2021) and public health (Collantes et al. 2015; Sánchez et al. 2021) perspective. In recent years, a few studies have provided reference NIS inventories and first assessments targeting different inland ecosystems (freshwater or transitional environments) and biotic groups, at Iberian, national (Spanish or Portuguese) and regional scales. For instance, García-Berthou et al. (2007) provided the first checklist of animal species naturalised in Iberian inland waters, and Cobo et al. (2010) provided a similar inventory for Galicia (Spain), adding plant species and comparing with other areas from the Iberian Peninsula. Aguiar and Ferreira (2013) conducted an overview of the available knowledge on invasive plants in Iberian rivers, whereas Rodríguez-Merino et al. (2017) focused on the potential distribution of non-native aquatic macrophytes in Iberian inland waters. Later, Anastácio et al. (2019) compiled records of animal NIS introduced across Portuguese freshwater ecosystems and provided a thorough assessment of the temporal introduction rate, native regions, reported impacts and legal coverage from both Portuguese and European lists of NIS. Muñoz-Mas and García- Berthou (2020) conducted a comprehensive review of aquatic non-indigenous fauna introduced in Iberian inland waters and compared temporal introduction rates between the Iberian Peninsula and two Iberian subregions (Portugal and Galicia). More recently, through a horizon scan exercise, Oficialdegui et al. (2023) have identified the most relevant NIS recorded or potential introductions to Iberian inland waters, but a relevant number of NIS that did not score high enough are missing from this list. Aquatic non-indigenous species in Iberian inland waters 21 Most of the above-mentioned studies retrieved NIS records exclusively from published scientific literature, thus overlooking grey literature and unpublished but validated NIS records from private inventories, institutional repositories and official databases. Because of time lags between detecting a NIS in the field and its corresponding publication (Zenetos et al. 2017), official online databases are currently essential resources for regularly updating NIS checklists and informing management policies more rapidly. Overall, NIS records concerning Iberian inland waters are scattered across several publications and data sources, thus posing a serious constraint for an integrated NIS management at different spatial scales. Moreover, they are often biased towards animal taxa and purely freshwater ecosystems, so studies concerning aquatic plants (e.g. Aguiar and Ferreira 2013) and transitional waters (Zorita et al. 2013; Cabral et al. 2020; Zamora‐ Marín et al. 2023) are scarce and conducted at local or regional scales. Hence, multitaxa inventories of NIS introduced in Iberian inland waters (both fresh and transitional waters) are needed, since they comprise key tools in decision-making with potential implications on NIS regulation policies at national (Spanish and Portuguese) and European levels (e.g. the European Union list of Invasive Alien Species of Union concern, hereafter “the Union list”). In fact, the EU regulation No 1143/2014 on the prevention and management of the introduction and spread of invasive alien species (IAS) recommends the EU Member States to provide updated checklists on NIS introduced in their territory and conduct a comprehensive analysis of the unintentional introduction and spread pathways of the IAS of Union concern (Piria et al. 2018). This study updates the information on aquatic NIS occurring in Iberian inland waters by combining knowledge from a diverse panel of experts with an extensive screening of published literature (both international and grey literature), online databases (e.g. GBIF, EASIN and CABI), and technical reports or off-line databases provided by environmental agencies. Through a broad multi-taxa approach including fungi, flora and fauna, this study aims (1) to provide an extensive and updated inventory of NIS introduced in Iberian inland waters, (2) to assess overall patterns in introduction pathways, native regions, and temporal introduction rates, and (3) to discuss the legal coverage of national (Spanish and Portuguese) and European IAS regulation. To make this study as robust as possible, this comprehensive assessment was conducted by an expert-consensus-based approach, which ensured a reliable checklist validation from a taxonomic and state-of- the-art viewpoint, since misidentification or distributional errors are common when no group-specific experts are involved in NIS multi-taxa studies (Zenetos et al. 2017). Methods Study area and target habitats The Iberian Peninsula is mostly comprised of the mainland territory of Spain and Portugal. This area is characterised by a wide climatic gradient which extends from the northwestern (temperate oceanic conditions expressed as high rainfall and humidity values, and low continentality) to the southeastern edge (Mediterranean semiarid Jose M. Zamora-Marín et al. / NeoBiota 89: 17–44 (2023) 22 conditions), including also large parts of the territory exposed to Mediterranean climate with higher continentality. The coastline of the Iberian Peninsula extends over 3,904 km across the Mediterranean Sea (1,670 km), the Atlantic Ocean (1,367 km) and the Cantabrian Sea (867 km). Most of the Iberian territory is framed within major river basins, some of them shared between Spain and Portugal (e.g. Guadiana, Tagus and Douro catchments). Following the European Water Framework Directive (hereafter, WFD) (EC 2000), we considered inland waters as those standing or flowing surface aquatic ecosystems (both fresh and transitional waters) placed across land boundaries. Hence, this term included typically lotic (i.e. rivers and streams) and lentic freshwater ecosystems (i.e. lakes, wetlands and reservoirs), small water bodies (i.e. ponds and pools) and transitional or estuarine aquatic systems influenced by freshwater inputs (i.e. marshlands, brackish waters, estuaries and coastal lagoons). Here, all these aquatic ecosystems were collectively considered and referred to as inland waters. Inland waters from the Balearic and Macaronesia (i.e. Canary Islands, Madeira and the Azores archipelagos) islands were excluded. Compiling records and attributes of NIS An integrative and structured approach based on multiple data sources was applied to generate a comprehensive up-to-date inventory of all aquatic NIS occurring in Iberian inland waters. Firstly, we compiled all available literature on NIS occurrence in Iberian inland waters, including articles published in indexed international journals, grey literature (e.g. articles in regional journals or bulletins), online databases and technical reports. For peer-reviewed literature, we made a query in the Web of Science to retrieve all potential publications focused on NIS in Iberian inland waters. Boolean search terms included all words related to NIS or potential synonyms (i.e. alien, allochthonous, exotic, introduced, invasive, non-native and non-indigenous), target environments (i.e. freshwater, transitional, reservoir/s, lake/s, pool/s, pond/s, river/s, stream/s, estuary/ies and coastal lagoon/s) and the study area (i.e. Iberia, Iberian Peninsula, Spain and Portugal). Resulting publications were screened to generate a list of NIS introduced in Iberian inland waters. This preliminary list of NIS was further complemented with records from grey literature, national technical reports and regional checklists, as well as from the following databases: the European Alien Species Information Network (EASIN; http://easin.jrc.ec.europa.eu), CABI´s Invasive Species Compendium (CABI-ISC; http://www.cabi.org/isc/), the Global Invasive Species Database (GISD; www.iucngisd.org), the EXOCAT database (http://exocatdb.creaf.cat/base_dades/#), the AquaNIS database (http://www.corpi.ku.lt/databases/aquanis/) and the Global Biodiversity Information Facility database (GBIF; http://www.gbif.org/). We recorded all aquatic NIS introduced in Iberian inland waters up to August 2022. We considered target taxa to be all those NIS able to live in freshwater and/or transitional waters at least during part of their life cycle. Aquatic taxa native from a given Iberian river basin but introduced in other Iberian catchments (i.e. translocated species) were excluded from our inventory. This preliminary list was agreed and validated Aquatic non-indigenous species in Iberian inland waters 23 by a panel of 65 experts in conservation biology and invasion science from Spain and Portugal, covering both types of target aquatic ecosystems (freshwater and transitional environments) and all biotic groups potentially containing aquatic NIS. Following previous studies (see Muñoz-Mas and García-Berthou 2020), taxa clearly introduced into Iberian inland waters with self-sustaining populations were classified as “established” (most commonly referred as “naturalized” in plants), whereas those non-indigenous taxa reported to occur in the study area but without known self-sustaining populations were classified as “uncertain” (most commonly referred as “casual” in plants). Taxa with unclear biogeographic history in the Iberian Peninsula (i.e. native/introduced status) were considered as “cryptogenic”. The recorded aquatic NIS were classified into five major biotic groups: vertebrates, invertebrates (both freeliving and symbionts), vascular plants, macroalgae and fungi. From the screened data sources, we searched and retrieved the following four relevant species-specific attributes for all recorded NIS: native regions, introduction pathways, year of introduction and functional group. Native regions for the recorded NIS were divided into nine geographic regions: Africa, Antarctica, temperate Asia, tropical Asia, Australasia, Europe, Pacific Ocean, North America, and South America. According to the Convention of Biological Diversity (CBD 2014) and as stated by the EU regulation (European Commission 2017), which complemented the classification of introduction pathways previously proposed by Hulme et al. (2008), we used the following seven major categories to characterise the introduction pathways: Release, Escape, Contaminant, Stowaway, Corridor, Unaided and Unknown. Whenever possible, the most probable introduction pathways were based on published literature for the Iberian Peninsula. For each recorded NIS, the year of introduction (i.e. first detection in the wild) in Europe and both Iberian countries was obtained. This date at European scale was mostly retrieved from EASIN, whereas at the national scale (for Spain and Portugal) was mainly retrieved from scientific literature providing first records for the Iberian Peninsula. When unreported in the literature, we applied a conservative approach and considered the year of the corresponding publication as the year of introduction, following Cobo et al. (2010) and Muñoz-Mas and García-Berthou (2020). In the case of host-specific alien invertebrate symbionts (e.g. Onchocleidus dispar), we considered the year of introduction to be that of the host. By contrast, in the case of generalist non-in- digenous parasites (e.g. Lernaea cyprinacea), which can be introduced with many host species (native or non-indigenous species), we considered the first detection year of the parasite. Additionally, we retrieved from EASIN the name of the country/ies where a given NIS was detected for the first time within Europe. Recorded NIS were also classified into the following nine functional groups: primary producers, herbivores, predators or parasites, detritivores, filter feeders, omnivores, xylophages, pollinators and polyphagous. Lastly, we screened the current regulation to assess the legal coverage of the recorded NIS. In particular, we checked the inclusion of NIS in the Union list, the Spanish IAS Catalogue (Royal Decree 630/2013, latest update 1 December 2020), the Spanish Allochthonous List (Royal Decree 570/2020), and the Portuguese List of IAS (Decree-Law 92/2019). Jose M. Zamora-Marín et al. / NeoBiota 89: 17–44 (2023) 24 Data analyses We analysed which native regions, introduction pathways and functional groups were most prevalent for the recorded NIS. To avoid overrepresentation of those NIS associated with two or more categories, data on these attributes were down-weighted in frequencyrelated analyses following the strategy of Muñoz-Mas and García-Berthou (2020). We used data on the first year of introduction of the recorded NIS in Europe, Spain and Portugal to compare temporal trends. We also applied linear models to assess pairwise differences in introduction dates among both Iberian countries and Europe (e.g. Spain vs Europe) and to determine potential NIS introduction delays. Lastly, legal coverage of the listed NIS in the official European, Spanish and Portuguese regulation lists of NIS was visually assessed through Venn diagrams, obtained with the package VennDiagram (Chen 2022), implemented in the free software R v.4.0.3 (R Core Team 2022). Results Taxonomic approach We recorded 326 non-indigenous taxa in Iberian inland waters, which included 215 clearly established, 96 uncertain and 15 cryptogenic taxa (Suppl. material 1). The listed aquatic NIS represented five major biotic groups, with invertebrates (54.6% of total taxa) being the dominant one, followed by vertebrates (24.5%), vascular plants (12.6%), macroalgae (7.4%) and fungi (0.9%). These aquatic NIS covered virtually all phyla (15) inhabiting Iberian inland waters, and belonged to 36 classes. The most represented phyla (or division in the case of plants) were Chordata (27.0%), Arthropoda (20.6%) and Mollusca (16.0%), whereas Magnoliophyta (10.7%), Rhodophyta (6.1%), Platyhelminthes (5.5%) and Annelida (5.2%) gathered a lower number of NIS, and the remaining phyla showed marginal values (≤ 2%) (Fig. 1). Overall, the ratio established/total NIS was congruent across all biotic groups, with the speciesrichest phyla having a greatest number of established NIS (range 47–94% of established taxa from the total NIS richness). At lower taxonomic resolution, Actinopterygii (14.1%) was the class with most species among all the taxa recorded, followed by Magnoliopsida (10.7%), Malacostraca (9.2%), Gastropoda (8.3%), Bivalvia (7.4%) and Florideophyceae (6.1%) (Suppl. material 2: fig. S1). Most of the aquatic non-indigenous vertebrates (57.5%) were fish (Class Actinopterygii) and they mainly corresponded to NIS well established in Iberian inland waters (34 established; 12 uncertain taxa), with Cyprinidae being the dominant among the 16 recorded families (16 cyprinids out of 46 listed non-indigenous fish species). Reptiles were the second species-richest class among vertebrates (13 NIS, 16.2% of vertebrates) and they were exclusively represented by freshwater turtle species, with only one taxon being clearly established (Trachemys scripta). A similar pattern was found in birds and amphibians, with eight listed NIS for both classes but only two species of birds (Alopochen aegyptiaca and Cairina moschata) and three species of amphibians Aquatic non-indigenous species in Iberian inland waters 25 (Discoglossus pictus, Pelophylax kl. grafi and Xenopus laevis), respectively, were considered as established. On the other hand, the recorded non-indigenous invertebrates were represented by a widely diversified set of species that corresponded to 24 classes including 62 orders. Podocopida (19 NIS) and Decapoda (16 NIS) were the invertebrate orders with most species. Regarding vascular plants, our inventory included submerged, floating and emergent aquatic plants occurring in Iberian inland waters, which generally corresponded to hydrophytes and helophytes. Magnoliopsida (35 NIS) was the dominant group of vascular plants, 12 of these species belonging to the order Alismatales, whereas the class Polypodiopsida hosted three non-indigenous pteridophytes. Among macroalgae, Rhodophyta was the dominant group (20 NIS), whereas Ochrophyta (4 NIS) was much less represented. Lastly, non-indigenous fungi species (3 NIS) were exclusively represented by pathogens belonging to the genera Batrachochytrium and Aphanomyces, which mostly affect amphibians and crayfish, respectively. Native regions Native regions of the recorded NIS corresponded to all geographic areas, with the exception of Antarctica (Fig. 2). North America (26.8%) and temperate Asia (18.8%) were the most common native regions of Iberian aquatic NIS. We found 197 NIS (60.8%) that were native to a single geographic region (Suppl. material 2: fig. S2a). Overall, NIS belonging to all biotic groups were native to a wide variety of geographic regions (Fig. 2). Particularly, vertebrates were mostly native to North America, Europe and temperate Asia, whereas invertebrates were native to all geographic regions and they comprised Figure 1. Cross-group richness of aquatic non-indigenous species (NIS) recorded in inland waters (including freshwater and transitional waters) from the Iberian Peninsula. Groups correspond to phyla (animals) or divisions (plants). Colours refer to the proportion of NIS belonging to each establishment stage (established, uncertain or cryptogenic). From top to bottom, groups are ranked from the species-richest to the species-poorest. Jose M. Zamora-Marín et al. / NeoBiota 89: 17–44 (2023) 32 Patterns in aquatic NIS introduction Aquatic non-indigenous vertebrates and invertebrates were generally native to North America and temperate Asia, though a relevant proportion of taxa were also originated from Europe, being all these patterns congruent with previous studies (Anastácio et al. 2019; Muñoz-Mas and García-Berthou 2020). For vertebrates, this pattern was mainly due to the high number of non-indigenous fish species native to North America, Asia and Europe, which have been intentionally introduced (i.e. released) in Iberian inland waters to promote recreational fishing (García-Berthou et al. 2007). Most of these introduced fish corresponded to large piscivorous species (e.g. Micropterus salmoides and Esox lucius) and small-sized fish (e.g. Alburnus alburnus and Abramis bjoerkna) used as forage species for non-indigenous piscivores (Elvira and Almodóvar 2001). A non-negligible number of non-indigenous fish have also been intentionally released for ornamental purposes (e.g. Carassius auratus) or as a consequence of the aquarium trade (e.g. Aphanius fasciatus, Poecilia reticulata and Misgurnus bipartitus) (Maceda-Veiga et al. 2013; Clavero et al. 2023), whereas few of them became naturalised through escapes from fish farm facilities (e.g. Ictalurus punctatus) (Elvira and Almodóvar 2001; Maceda-Veiga et al. 2013). Nonindigenous fish introduced in Iberian inland waters but native to Europe are of particular interest because they have arrived through diverse introduction pathways, either intentionally as described above, or following a clear introduction route from French to northeastern Iberian basins (Clavero and García-Berthou 2006). The remaining non-indige- nous vertebrates were evenly native to all the considered regions (Suppl. material 2: fig. S8a), though non-indigenous reptiles were mostly native to North America, as previously documented for Spain (Vilà et al. 2001; Poch et al. 2020). However, this pattern in reptile introductions contrasts with that reported for non-indigenous herpetofauna naturalised in Europe, which was mostly native to Asia and Africa (Kark et al. 2009). Overall, non-indig- enous vertebrates were almost exclusively introduced through intentional pathways (i.e. release and escape) (Suppl. material 2: fig. S8b), which is in accordance with continental patterns reported for Europe (Nunes et al. 2015; Saul et al. 2017). Native biogeographic regions for non-indigenous vertebrates correspond to temperate regions with climate regimes similar to the Iberian Peninsula. In this context, NIS introductions from regions with similar climate regimes are more likely to be successful and lead to established NIS (i.e. self-sustaining populations), as these species could be physiologically already adapted to the environmental conditions of the recipient aquatic ecosystems (Ribeiro et al. 2008). Unlike vertebrates, invertebrate NIS were mostly introduced in Iberian inland waters through two unintentional pathways: contaminant and stowaway. They were native to almost all geographic regions, with North America and temperate Asia being the predominant. Previous studies have shown that most estuarine NIS of non-mollusc and nonarthropod invertebrates (e.g. annelids or platyhelminthes) reached the Iberian coast as hitchhikers through ballast water or hull fouling vessels from global maritime trade (Zorita et al. 2013; Chainho et al. 2015; López and Richter 2017; Cabral et al. 2020). This vector of introduction has been also highlighted as responsible for the arrival of some arthropods (e.g. estuarine crabs) to Iberian transitional waters. Several non-indigenous invertebrates Aquatic non-indigenous species in Iberian inland waters 33 (e.g. ostracods) have been also passively imported with rice culturing from Asia (Forès 1998; Valls et al. 2014). Non-indigenous decapods were composed by two separate groups, with freshwater crayfish being mostly native to North America and introduced intentionally (i.e. escape or release) for commercial purposes (Vedia and Miranda 2013), whereas estuarine crabs arrived unintentionally through stowaway and were mostly native to America (Muñoz-Mas and García-Berthou 2020). Non-indigenous molluscs arrived to Iberian inland waters mostly through stowaway, contaminants and escape, most of them associated with aquaculture facilities (López-Soriano and Quiñonero-Salgado 2016). The opening and subsequent enlargement of the Suez Canal in 1869 also allowed several estuarine gastropods of Indo-Pacific origin (the so-called Lessepsian migrants) to colonise the Mediterranean Sea (Nunes et al. 2014), and spread over transitional waters of the Iberian coast. For instance, such is the case of the molluscs Fulvia fragilis, Bursatella leachii, Pinctada radiata and Cerithium scabridum (López-Soriano et al. 2020). Moreover, anthropogenic modifications of Iberian estuaries may facilitate the establishment of those NIS that are more environmentally tolerant (González-Ortegón and Moreno-Andrés 2021). The recorded non-indigenous aquatic vascular plants are mainly native to South and North America, and most of them were introduced through escape and release, although a non-negligible number of them also arrived as contaminants. Moreover, up to five different introduction pathways were exclusively associated with the arrival of some non-in- digenous aquatic plants (e.g. Heteranthera limosa) (Suppl. material 2: fig. S2b). This pattern in non-indigenous plant introduction is congruent with that reported at continental scale in Europe, with escape being the major introduction pathway and vascular plants being also the biotic group introduced through more diverse vectors (Pergl et al. 2017). Almost half of the recorded non-indigenous macroalgae was native to the Pacific Ocean and considered Lessepsian migrants, whereas the other half was native to the remaining geographic regions and introduced presumably passively through maritime traffic (Chainho et al. 2015; Orlando-Bonaca et al. 2021). Fungi corresponded to pathogens and were exclusively introduced as contaminants, but results provided here for this group are likely biased due to important challenges for taxonomic identification and poor knowledge of their biogeography (Bailey et al. 2020; Turbelin et al. 2022). Legal coverage and policy implications Legislative instruments (e.g. regulation lists or catalogues) are developed at European, national and even regional level to prevent the introduction and spread of enlisted NIS through direct management actions. The Regulation (EU) No 1143/2014 established a list of IAS of Union concern which entails that all EU Member States must implement specific management actions to prevent new introductions and further spread across European countries (Genovesi et al. 2015). Spain and Portugal have developed and adapted their IAS legislations to the EU Regulation, with the Spanish IAS catalogue and the Portuguese national IAS list being pivotal for providing legally binding lists that imply a generic prohibition on possession, transport and trade of listed taxa. We found that about 8% of the NIS recorded in Iberian inland waters were included in Jose M. Zamora-Marín et al. / NeoBiota 89: 17–44 (2023) 34 the Union list, which is the core of the EU Regulation. On the other hand, 26% and 25% of the recorded NIS were included in the Portuguese and Spanish IAS catalogues respectively, although it is understandable that the national IAS regulations do not necessarily include all the non-indigenous species recorded in their territories. Additionally, almost half (48.5%) of the listed NIS were also listed in the Spanish Allochthonous List, but this regularly upgraded list is focused on taxa potentially introduced in the near future and aims to regulate the importation of new NIS (other than those listed in the Union List and the Spanish IAS List) from other countries that are not part of the European Union and to promote adequate risk assessment. This moderately high percentage is explained by the fact that the Spanish Allochthonous List includes several entire genera (e.g. Alternanthera ssp. and Lepomis ssp.) and a very large number of species with the aim of regulating the potential importation of allochthonous taxa which are actually sibling species of already introduced NIS (e.g. Alternanthera sessilis and Lepomis gibbosus) and could lead to similar impacts in Iberian inland waters. About 17.6% of the listed NIS in the present study have their native range within Europe, thus placing important challenges for transnational regulation and cooperation at Europe scale. This situation may lead to a complex conservation paradox when some aquatic species are native and even threatened in certain EU Member States but they have been introduced and become invasive in others (Marchetti and Engstrom 2016). Hence, national-level regulation instruments must be properly designed and implemented to deal with NIS that are particularly harmful to a given region and address these inherent constraints derived from managing NIS at European scale (Baquero et al. 2023). Consequently, effective management will require that national NIS catalogues are complemented to include all taxa that are considered a priority for management (Angulo et al. 2021). In this context, horizon scan exercises may become particularly useful to identify those high-risk NIS requiring priority management actions within a given region. In fact, Oficialdegui et al. (2023) highlighted a concern list of 126 taxa (all of them included in our inventory making up 38.6% of our listed NIS), as the most relevant invasive alien species already present in Iberian inland waters. Despite the effort made in these kinds of exercises, further research is needed to update the lists, and to address other aquatic invasive taxa that are continually being reported for the first time. The inventory presented here may be useful for this purpose. On the other hand, our assessment on legal coverage provided by regulation lists highlighted important taxonomic-related biases. For instance, the Union list does not include any non-indigenous mollusc despite most of them being non-indigenous to Europe and some are already causing important ecological and economic impacts in Iberian inland waters (Sampaio and Rodil 2014; Gilioli et al. 2017). Therefore, further European-scale efforts should be done to include non-indigenous molluscs in NIS regulation. Although the Iberian Peninsula can be considered a single biogeographical entity, our results pointed to a considerable mismatch in the criteria followed for species listing between both Spanish and Portuguese catalogues. For instance, several NIS already introduced in both Iberian countries were included in the Spanish IAS catalogue but excluded from the Portuguese one, and vice versa. Hence, independent NIS management Aquatic non-indigenous species in Iberian inland waters 35 in neighbouring countries belonging to the same biogeographical region can jeopardise resource optimization and ultimately hinder effectiveness of management actions. Supra-national coordinated management actions are particularly needed, as they are generally more effective than national or regional ones (Faulkner et al. 2020). In fact, the Article 11 of the EU Regulation states that coordination and cooperation among MS is pivotal to address a strategic management. Owing to the several river basins shared by Spain and Portugal, the creation of an Iberian office for a coordinated NIS management would likely enhance the effectiveness of control measures and prevention protocols, as well as inter-sectorial communication for improving stakeholder engagement, as already suggested for other regions (Caffrey et al. 2014; Piria et al. 2017). Within the framework of this coordination office, national governments should channel management strategies on aquatic NIS through inter-regional regulation institutions (i.e. river basin authorities and coastal demarcations) to ensure coordinated efforts and avoid constraints from political borders among autonomous communities. The management of NIS is therefore a complex and transnational challenge that requires multi-faceted actions involving diverse institutions and stakeholders at different spatial scales (Baquero et al. 2021). For that purpose, the EU Regulation allows MS to list NIS of regional concern that require enhanced cooperation among involved countries. To inform these NIS management strategies, further research efforts in invasion science should be more applied and focused on cost-efficient actions (Muñoz-Mas et al. 2021). Conclusions The introduction of NIS in Iberian inland waters is a long-lasting process affecting many facets of biodiversity, but also local economies and public health. Managing aquatic NIS in the Iberian Peninsula requires a well-coordinated strategy among decision-makers and stakeholders. Nowadays, the increase of human pressure on natural habitats, the climate change and the expanding international trade are promoting the entry, spread, and establishment of new non-native taxa, particularly in inland waters. Hence, effective NIS management requires updated and detailed information on main introduction-related attributes. This study provides a comprehensive multi-taxa inventory of aquatic NIS introduced in Iberian freshwater and transitional waters. This baseline information is delivered through a freely available database intended to become a key tool for improving NIS prevention, monitoring and management at Iberian level. For instance, our assessment may serve as a useful resource for managing NIS introduction pathways into freshwater and estuarine ecosystems, as well as for communicating the magnitude of aquatic invasions to all related authorities and stakeholders. Moreover, this inventory also aims to meet the requirements on updated NIS data stated by the EU Regulation on IAS. Ultimately, our study provides valuable information on the implementation of other EU policies with implications on NIS management, such as the EU Biodiversity Strategy to 2030, the Birds and Habitats Directives, the Marine Strategy Framework Directive, and the Water Framework Directive. Jose M. Zamora-Marín et al. / NeoBiota 89: 17–44 (2023) 36 Funding This study was supported by the LIFE INVASAQUA project (Aquatic Invasive Alien Species of Freshwater and Estuarine Systems: Awareness and Prevention in the Iberian Peninsula) (LIFE17 GIE/ES/000515) funded by the EU LIFE Program. The Fundación Biodiversidad (Government of Spain) and the Government of Navarre financially supported specific actions into the LIFE INVASAQUA. J.M. Z.-M. is supported by a postdoctoral grant funded by the Spanish Ministry of Science and Innovation and the European Union NextGeneration EU/PRTR (FJC2021-046923-I). F.R. is supported by Foundation for Science and Technology through an individual contract (CEEC/0482/2020). I.B. and J.A.C. were funded by the Basque Government (IT1487-22). J.E. has a Ph.D. scholarship (SFRH/BD/140556/2018) funded by FCT, Portugal. F.B. is supported by Foundation for Science and Technology through an individual contract (CEEC/01896/2021). C.C. was supported by Portuguese national funds to the CEG/IGOT Research Unit (UIDB/00295/2020 and UIDP/00295/2020), through FCT - Fundação para a Ciência e a Tecnologia, I.P. F.C.A, was funded by CEF, a research unit of FCT, Portugal (UIDB/00239/2020). A.A. H.-R. was supported by a predoctoral grant from the University of Murcia (R-483/2023). CRediT author statement Conceptualization & Coordinating groups: FJ Oliva-Paterna, JM Zamora-Marín, F Ribeiro, PM Anastácio, B Gallardo, E García-Berthou, P García-Murillo, F Cobo, R Miranda, D Boix, L Medina, F Morcillo, J Oscoz, A Guillén, A Arias, JA Cuesta. Data curation: A Ruiz-Navarro, F Ribeiro, AA Herrero-Reyes, JM Zamora-Marín and FJ Oliva-Paterna. Formal analyses: JM Zamora-Marín, A Ruiz-Navarro, A Guerrero-Gómez and FJ Oliva-Paterna. Writing - Original draft: JM Zamora-Marín, A Ruiz-Navarro, FJ Oliva-Paterna, FJ Oficialdegui. Supervision and Writing - review & editing: FJ Oliva-Paterna, JM Zamora-Marín, FJ Oficialdegui, F Ribeiro, PM Anastácio, B Gallardo, E García-Berthou, P García-Murillo, R Miranda, D Boix, A Arias, JA Cuesta. Investigation, Visualization & Review: All authors. Project Administration: FJ Oliva-Paterna. All authors have reviewed and contributed to improve the text and figures. Acknowledgements We thank many experts who have contributed to this NIS inventory by providing useful records, suggestions and opinions through personal communications: Núria Bonada, Ramón De Miguel, Estibaliz Díaz, Ignacio Doadrio, Rocío Fernández-Zamudio, Nati Franch, Pedro M. Guerreiro, Emilio Laguna, Pedro Leunda, Francisco Martínez- Capel, José A. Molina, Jorge Paiva, Angel Pérez-Ruzafa, Carla Pinto and Manuel Toro. Aquatic non-indigenous species in Iberian inland waters 37 References Aguiar FCF, Ferreira MT (2013) Plant invasions in the rivers of the Iberian Peninsula, southwestern Europe: A review. Plant Biosystems 147(4): 1107–1119. https://doi.org/10.1080 /11263504.2013.861539 Anastácio PM, Ribeiro F, Capinha C, Banha F, Gama M, Filipe AF, Rebelo R, Sousa R (2019) Non-native freshwater fauna in Portugal: A review. The Science of the Total Environment 650: 1923–1934. https://doi.org/10.1016/j.scitotenv.2018.09.251 Angulo E, Ballesteros-Mejia L, Novoa A, Duboscq-Carra VG, Diagne C, Courchamp F (2021) Economic costs of invasive alien species in Spain. NeoBiota 67: 267–297. https://doi. org/10.3897/neobiota.67.59181 Araújo MB, Lobo JM, Moreno JC (2007) The effectiveness of Iberian protected areas in conserving terrestrial biodiversity. Conservation Biology 21(6): 1423–1432. https://doi. org/10.1111/j.1523-1739.2007.00827.x Bailey SA, Brown L, Campbell ML, Canning-Clode J, Carlton JT, Castro N, Chainho P, Chan FT, Creed JC, Curd A, Darling J, Fofonoff P, Galil BS, Hewitt CL, Inglis GJ, Keith I, Mandrak NE, Marchini A, McKenzie CH, Occhipinti-Ambrogi A, Ojaveer H, Pires-Teixeira LM, Robinson TB, Ruiz GM, Seaward K, Schwindt E, Son MO, Therriault TW, Zhan A (2020) Trends in the detection of aquatic non-indigenous species across global marine, estuarine and freshwater ecosystems: A 50-year perspective. Diversity & Distributions 26(12): 1780–1797. https://doi.org/10.1111/ddi.13167 Baquero R, Ayllón D, Oficialdegui F, Nicola G (2021) Tackling biological invasions in Natura 2000 network in the light of the new EU Biodiversity Strategy for 2030. Management of Biological Invasions 12(4): 776–791. https://doi.org/10.3391/mbi.2021.12.4.01 Baquero RA, Oficialdegui FJ, Ayllón D, Nicola GG (2023) The challenge of managing threatened invasive species at a continental scale. Conservation Biology 37(5): 16–23. https:// doi.org/10.1111/cobi.14165 Britton JR, Lynch AJ, Bardal H, Bradbeer SJ, Coetzee JA, Coughlan NE, Dalu T, Tricarico E, Gallardo B, Lintermans M, Lucy F, Liu C, Olden JD, Raghavan R, Pritchard EG (2023) Preventing and controlling nonnative species invasions to bend the curve of global freshwater biodiversity loss. Environmental Reviews 31(2): 310–326. https://doi.org/10.1139/er-2022-0103 Buira A, Aedo C, Medina L (2017) Spatial patterns of the Iberian and Balearic endemic vascular flora. Biodiversity and Conservation 26(2): 479–508. https://doi.org/10.1007/s10531- 016-1254-z Cabral S, Carvalho F, Gaspar M, Ramajal J, Sá E, Santos C, Silva G, Sousa A, Costa JL, Chainho P (2020) Non-indigenous species in soft-sediments: Are some estuaries more invaded than others? Ecological Indicators 110: 105640. https://doi.org/10.1016/j.ecolind.2019.105640 Caffrey J, Baars J-R, Barbour J, Boets P, Boon P, Davenport K, Dick J, Early J, Edsman L, Gallagher C, Gross J, Heinimaa P, Horrill C, Hudin S, Hulme P, Hynes S, MacIsaac H, McLoone P, Millane M, Moen T, Moore N, Newman J, O’Conchuir R, O’Farrell M, O’Flynn C, Oidtmann B, Renals T, Ricciardi A, Roy H, Shaw R, Weyl O, Williams F, Lucy F (2014) Tackling Invasive Alien Species in Europe: The top 20 issues. Management of Biological Invasions 5(1): 1–20. https://doi.org/10.3391/mbi.2014.5.1.01 Jose M. Zamora-Marín et al. / NeoBiota 89: 17–44 (2023) 38 Capinha C, Essl F, Porto M, Seebens H (2023) The worldwide networks of spread of recorded alien species. Proceedings of the National Academy of Sciences 120(1): e2201911120. https://doi.org/10.1073/pnas.2201911120 CBD (2014) Pathways of introduction of invasive species, their prioritization and management. https://www.cbd.int/doc/meetings/sbstta/sbstta-18/official/sbstta-18-09-add1-en.pdf Chainho P, Fernandes A, Amorim A, Ávila SP, Canning-Clode J, Castro JJ, Costa AC, Costa JL, Cruz T, Gollasch S, Grazziotin-Soares C, Melo R, Micael J, Parente MI, Semedo J, Silva T, Sobral D, Sousa M, Torres P, Veloso V, Costa MJ (2015) Non-indigenous species in Portuguese coastal areas, coastal lagoons, estuaries and islands. Estuarine, Coastal and Shelf Science 167: 199–211. https://doi.org/10.1016/j.ecss.2015.06.019 Chen H (2022) VennDiagram: Generate High-Resolution Venn and Euler Plots. https:// cran.r-project.org/package=VennDiagram Clavero M, García-Berthou E (2006) Homogenization dynamics and introduction routes of invasive freshwater fish in the Iberian Peninsula. Ecological Applications 16(6): 2313– 2324. https://doi.org/10.1890/1051-0761(2006)016[2313:HDAIRO]2.0.CO;2 Clavero M, Suh J, Franch N, Aparicio E, Buchaca T, Caner J, Garcia‐Rodriguez S, Llimona F, Pou‐Rovira Q, Rocaspana R, Ventura M (2023) Invaders they are a‐changing†: A recent, unexpected surge of invasive loaches in Catalonia. Freshwater Biology 68(4): 621–631. https://doi.org/10.1111/fwb.14051 Cobo F, Vieira-Lanero R, Rego E, Servia MJ (2010) Temporal trends in non-indigenous freshwater species records during the 20th century: A case study in the Iberian Peninsula. Biodiversity and Conservation 19(12): 3471–3487. https://doi.org/10.1007/s10531-010-9908-8 Collantes F, Delacour S, Alarcón-Elbal PM, Ruiz-Arrondo I, Delgado JA, Torrell-Sorio A, Bengoa M, Eritja R, Miranda MÁ, Molina R, Lucientes J (2015) Review of ten-years presence of Aedes albopictus in Spain 2004–2014: Known distribution and public health concerns. Parasites & Vectors 8(1): 655. https://doi.org/10.1186/s13071-015-1262-y Cruz MJ, Segurado P, Sousa M, Rebelo R (2008) Collapse of the amphibian community of the Paul do Boquilobo Natural Reserve (central Portugal) after the arrival of the exotic American crayfish Procambarus clarkii. The Herpetological Journal 18: 197–204. Doadrio I, Perea S Garzón-Heydt, González JL (2011) Ictiofauna continental española. Bases para su seguimiento. Madrid, Spain. Durán C, Lanao M, Pérez y Pérez L, Chica C, Anadón A, Touya V (2012) Estimación de los costes de la invasión del mejillón cebra en la cuenca del Ebro (periodo 2005–2009). Limnetica 31(2): 213–230. https://doi.org/10.23818/limn.31.20 Elvira B, Almodóvar A (2001) Freshwater fish introductions in Spain: Facts and figures at the beginning of the 21st century. Journal of Fish Biology 59(sA): 323–331. https://doi. org/10.1111/j.1095-8649.2001.tb01393.x European Commission (2000) Common Implementation Strategy for the Water Framework Directive (2000/60/EC). Publication Office of the European Union, Luxembourg. Faulkner KT, Robertson MP, Wilson JRU (2020) Stronger regional biosecurity is essential to prevent hundreds of harmful biological invasions. Global Change Biology 26(4): 2449– 2462. https://doi.org/10.1111/gcb.15006 Forès E (1998) Els ostràcodes dels arrossars del delta de l’Ebre: Sistemàtica, ecologia i distribució geogràfica. Bulletí de la Institució Catalana d’Historia Natural 7: 47–57. Aquatic non-indigenous species in Iberian inland waters 39 Fuentes N, Marticorena A, Saldaña A, Jerez V, Ortiz JC, Victoriano P, Moreno RA, Larraín J, Villaseñor-Parada C, Palfner G, Sánchez P, Pauchard A (2020) Multi-taxa inventory of naturalized species in Chile. NeoBiota 60: 25–41. https://doi.org/10.3897/neobiota.60.55366 Gallardo B, Clavero M, Sánchez MI, Vilà M (2016) Global ecological impacts of invasive species in aquatic ecosystems. Global Change Biology 22(1): 151–163. https://doi. org/10.1111/gcb.13004 García-Berthou E, Boix D, Clavero M (2007) Non-indigenous animal species naturalized in Iberian inland waters. In: Springer (Ed.) Biological invaders in inland waters: Profiles, distribution, and threatsI. Invading Nature: Springer Series in Invasion Ecology. Springer, Dordrecht, Netherlands, 123–140. https://doi.org/10.1007/978-1-4020-6029-8_6 Genovesi P, Carboneras C, Vilà M, Walton P (2015) EU adopts innovative legislation on invasive species: A step towards a global response to biological invasions? Biological Invasions 17(5): 1307–1311. https://doi.org/10.1007/s10530-014-0817-8 Gilioli G, Schrader G, Carlsson N, van Donk E, van Leeuwen CHA, Martín PR, Pasquali S, Vilà M, Vos S (2017) Environmental risk assessment for invasive alien species: A case study of apple snails affecting ecosystem services in Europe. Environmental Impact Assessment Review 65: 1–11. https://doi.org/10.1016/j.eiar.2017.03.008 González-Ortegón E, Moreno-Andrés J (2021) Anthropogenic modifications to estuaries facilitate the invasion of non-native species. Processes 9(5): 740. https://doi.org/10.3390/pr9050740 Guareschi S, Laini A, England J, Barrett J, Wood PJ (2021) Multiple co‐occurrent alien invaders constrain aquatic biodiversity in rivers. Ecological Applications 31(6): e02385. https:// doi.org/10.1002/eap.2385 Hermoso V, Filipe AF, Segurado P, Beja P (2016) Catchment zoning to unlock freshwater conservation opportunities in the Iberian Peninsula. Diversity and Distributions 22: 960–969. https://doi.org/10.1111/ddi.12454 Hulme PE, Bacher S, Kenis M, Klotz S, Kühn I, Minchin D, Nentwig W, Olenin S, Panov V, Pergl J, Pyšek P, Roques A, Sol D, Solarz W, Vilà M (2008) Grasping at the routes of biological invasions: A framework for integrating pathways into policy. Journal of Applied Ecology 45(2): 403–414. https://doi.org/10.1111/j.1365-2664.2007.01442.x Kark S, Solarz W, Chiron F, Clergeau P, Shirley S (2009) Alien birds, amphibians and reptiles of Europe. In: Handbook of Alien Species in Europe. Invading Nature - Springer Series in Invasion Ecology, vol 3. Springer, Dordrecht, 105–118. https://doi.org/10.1007/978-1-4020-8280-1_8 Katsanevakis S, Coll M, Piroddi C, Steenbeek J, Lasram FBR, Zenetos A, Cardoso AC (2014) Invading the Mediterranean Sea: Biodiversity patterns shaped by human activities. Frontiers in Marine Science 1: 1–11. https://doi.org/10.3389/fmars.2014.00032 Lonsdale W (1999) Global patterns of plant invasions and the concept of invasibility. Ecology 80(5): 1522–1536. https://doi.org/10.1890/0012-9658(1999)080[1522:GPOPIA]2.0.CO;2 López E, Richter A (2017) Non-indigenous species (NIS) of polychaetes (Annelida: Polychaeta) from the Atlantic and Mediterranean coasts of the Iberian Peninsula: An annotated checklist. Helgoland Marine Research 71(1): 19. https://doi.org/10.1186/s10152-017-0499-6 López-Soriano J, Quiñonero-Salgado S (2016) Malacofauna alóctona asociada a la acuicultura marina. Spira 6: 67–77. López-Soriano J, Quiñonero-Salgado S, Forner E, Verdejo Guirao JA, Murcia Requena J (2020) Consolidación de las poblaciones ibéricas del invasor lessepsiano Jose M. Zamora-Marín et al. / NeoBiota 89: 17–44 (2023) 40 Cerithium scabridum Philippi, 1848 (Gastropoda: Cerithiidae). Elona. Revista de Malacología Ibérica 1: 98–101. Maceda-Veiga A, Escribano-Alacid J, de Sostoa A, García-Berthou E (2013) The aquarium trade as a potential source of fish introductions in southwestern Europe. Biological Invasions 15(12): 2707–2716. https://doi.org/10.1007/s10530-013-0485-0 Marchetti MP, Engstrom T (2016) The conservation paradox of endangered and invasive species. Conservation Biology 30(2): 434–437. https://doi.org/10.1111/cobi.12642 McFadden IR, Sendek A, Brosse M, Bach PM, Baity‐Jesi M, Bolliger J, Bollmann K, Brockerhoff EG, Donati G, Gebert F, Ghosh S, Ho H, Khaliq I, Lever JJ, Logar I, Moor H, Odermatt D, Pellissier L, de Queiroz LJ, Rixen C, Schuwirth N, Shipley JR, Twining CW, Vitasse Y, Vorburger C, Wong MKL, Zimmermann NE, Seehausen O, Gossner MM, Matthews B, Graham CH, Altermatt F, Narwani A (2023) Linking human impacts to community processes in terrestrial and freshwater ecosystems. Ecology Letters 26(2): 203–218. https://doi.org/10.1111/ele.14153 McGeoch MA, Spear D, Kleynhans EJ, Marais E (2012) Uncertainty in invasive alien species listing. Ecological Applications 22(3): 959–971. https://doi.org/10.1890/11-1252.1 Moorhouse TP, Macdonald DW (2015) Are invasives worse in freshwater than terrestrial ecosystems? WIREs. Water 2(1): 1–8. https://doi.org/10.1002/wat2.1059 Muñoz-Mas R, García-Berthou E (2020) Alien animal introductions in Iberian inland waters: An update and analysis. The Science of the Total Environment 703: 134505. https://doi. org/10.1016/j.scitotenv.2019.134505 Muñoz-Mas R, Carrete M, Castro-Díez P, Delibes-Mateos M, Jaques JA, López-Darias M, Nogales M, Pino J, Traveset A, Turon X, Vilà M, García-Berthou E (2021) Management of invasive alien species in Spain: A bibliometric review. NeoBiota 70: 123–150. https:// doi.org/10.3897/neobiota.70.68202 Nunes AL, Katsanevakis S, Zenetos A, Cardoso AC (2014) Gateways to alien invasions in the European seas. Aquatic Invasions 9(2): 133–144. https://doi.org/10.3391/ai.2014.9.2.02 Nunes A, Tricarico E, Panov V, Cardoso A, Katsanevakis S (2015) Pathways and gateways of freshwater invasions in Europe. Aquatic Invasions 10(4): 359–370. https://doi. org/10.3391/ai.2015.10.4.01 Oficialdegui FJ, Zamora-Marín JM, Guareschi S, Anastácio PM, García-Murillo P, Ribeiro F, Miranda R, Cobo F, Gallardo B, García-Berthou E, Boix D, Arias A, Cuesta JA, Medina L, Almeida D, Banha F, Barca S, Biurrun I, Cabezas MP, Calero S, Campos JA, Capdevila- Argüelles L, Capinha C, Casals F, Clavero M, Encarnação J, Fernández-Delgado C, Franco J, Guillén A, Hermoso V, Machordom A, Martelo J, Mellado-Díaz A, Morcillo F, Oscoz J, Perdices A, Pou-Rovira Q, Rodríguez-Merino A, Ros M, Ruiz-Navarro A, Sánchez MI, Sánchez-Fernández D, Sánchez-González JR, Sánchez-Gullón E, Teodósio MA, Torralva M, Vieira-Lanero R, Oliva-Paterna FJ (2023) A horizon scan exercise for aquatic invasive alien species in Iberian inland waters. The Science of the Total Environment 869: 161798. https://doi.org/10.1016/j.scitotenv.2023.161798 Ojaveer H, Galil BS, Carlton JT, Alleway H, Goulletquer P, Lehtiniemi M, Marchini A, Miller W, Occhipinti-Ambrogi A, Peharda M, Ruiz GM, Williams SL, Zaiko A (2018) Historical baselines in marine bioinvasions: Implications for policy and management. PLoS ONE 13(8): e0202383. https://doi.org/10.1371/journal.pone.0202383 Aquatic non-indigenous species in Iberian inland waters 41 Orlando-Bonaca M, Lipej L, Bonanno G (2021) Non-indigenous macrophytes in Central Mediterranean ports, marinas and transitional waters: Origin, vectors and pathways of dispersal. Marine Pollution Bulletin 162: 111916. https://doi.org/10.1016/j.marpolbul.2020.111916 Pergl J, Pyšek P, Bacher S, Essl F, Genovesi P, Harrower CA, Hulme PE, Jeschke JE, Kenis M, Kühn I, Perglová I, Rabitsch W, Roques A, Roy DB, Roy HE, Vilà M, Winter M, Nentwig W (2017) Troubling travellers: Are ecologically harmful alien species associated with particular introduction pathways? NeoBiota 32: 1–20. https://doi.org/10.3897/neobiota.32.10199 Piria M, Copp G, Dick J, Duplić A, Groom Q, Jelić D, Lucy F, Roy H, Sarat E, Simonović P, Tomljanović T, Tricarico E, Weinlander M, Adámek Z (2017) Tackling invasive alien species in Europe II: Threats and opportunities until 2020. Management of Biological Invasions 8(3): 273–286. https://doi.org/10.3391/mbi.2017.8.3.02 Piria M, Simonović P, Kalogianni E, Vardakas L, Koutsikos N, Zanella D, Ristovska M, Apostolou A, Adrović A, Mrdak D, Tarkan AS, Milošević D, Zanella LN, Bakiu R, Ekmekçi FG, Povž M, Korro K, Nikolić V, Škrijelj R, Kostov V, Gregori A, Joy MK (2018) Alien freshwater fish species in the Balkans—Vectors and pathways of introduction. Fish and Fisheries 19(1): 138–169. https://doi.org/10.1111/faf.12242 Poch S, Sunyer P, Pascual G, Boix D, Campos M, Cruset E, Quer-Feo C, Fuentes MA, Molina A, Porcar A, Pérez-Novo I, Pou‐Rovira Q, Ramos S, Escoriza D (2020) Alien chelonians in north-eastern Spain: New distributional data. Herpetological Bulletin 151(151, Spring 2020): 1–5. https://doi.org/10.33256/hb151.15 R Core Team (2022) R: a language and environment for statistical computing. Vienna, Austria. https://www.r-project.org/ Reid AJ, Carlson AK, Creed IF, Eliason EJ, Gell PA, Johnson PTJ, Kidd KA, MacCormack TJ, Olden JD, Ormerod SJ, Smol JP, Taylor WW, Tockner K, Vermaire JC, Dudgeon D, Cooke SJ (2019) Emerging threats and persistent conservation challenges for freshwater biodiversity. Biological Reviews of the Cambridge Philosophical Society 94(3): 849–873. https://doi.org/10.1111/brv.12480 Ribeiro F, Elvira B, Collares-Pereira MJ, Moyle PB (2008) Life-history traits of non-native fishes in Iberian watersheds across several invasion stages: A first approach. Biological Invasions 10(1): 89–102. https://doi.org/10.1007/s10530-007-9112-2 Rodríguez-Merino A, Fernández-Zamudio R, García-Murillo P (2017) An invasion risk map for non-native aquatic macrophytes of the Iberian Peninsula. Anales del Jardín Botánico de Madrid 74: 055. https://doi.org/10.3989/ajbm.2452 Rodríguez-Merino A, García-Murillo P, Cirujano S, Fernández-Zamudio R (2018) Predicting the risk of aquatic plant invasions in Europe: How climatic factors and anthropogenic activity influence potential species distributions. Journal for Nature Conservation 45: 58–71. https://doi.org/10.1016/j.jnc.2018.08.007 Romero R (2015) Depredación de visón americano sobre desmán ibérico en Galicia. Galemys. Galemys 27: 13–22. https://doi.org/10.7325/Galemys.2015.A2 Rosso A, Aragón P, Acevedo F, Doadrio I, García-Barros E, Lobo JM, Munguira ML, Monserrat VJ, Palomo J, Pleguezuelos JM, Romo H, Triviño V, Sánchez-Fernández D (2018) Effectiveness of the Natura 2000 network in protecting Iberian endemic fauna. Animal Conservation 21(3): 262–271. https://doi.org/10.1111/acv.12387